Margaret A. Stanton

Social networks reveal cultural behaviour in tool-using dolphins

Animal tool use is of inherent interest given its relationship to intelligence, innovation and cultural behaviour. Here we investigate whether Shark Bay bottlenose dolphins that use marine sponges as hunting tools (spongers) are culturally distinct from other dolphins in the population based on the criteria that sponging is both socially learned and distinguishes between groups. We use social network analysis to determine social preferences among 36 spongers and 69 non-spongers sampled over a 22-year period while controlling for location, sex and matrilineal relatedness. Homophily (the tendency to associate with similar others) based on tool-using status was evident in every analysis, although maternal kinship, sex and location also contributed to social preference. Female spongers were more cliquish and preferentially associated with other spongers over non-spongers. Like humans who preferentially associate with others who share their subculture, tool-using dolphins prefer others like themselves, strongly suggesting that sponge tool-use is a cultural behaviour.

Early Social Networks Predict Survival in Wild Bottlenose Dolphins

A fundamental question concerning group-living species is what factors influence the evolution of sociality. Although several studies link adult social bonds to fitness, social patterns and relationships are often formed early in life and are also likely to have fitness consequences, particularly in species with lengthy developmental periods, extensive social learning, and early social bond-formation. In a longitudinal study of bottlenose dolphins (Tursiops sp.), calf social network structure, specifically the metric eigenvector centrality, predicted juvenile survival in males. Additionally, male calves that died post-weaning had stronger ties to juvenile males than surviving male calves, suggesting that juvenile males impose fitness costs on their younger counterparts. Our study indicates that selection is acting on social traits early in life and highlights the need to examine the costs and benefits of social bonds during formative life history stages.

Boys will be boys: sex differences in wild infant chimpanzee social interactions

Sex differences in the behaviour of human children are a hotly debated and often controversial topic. However, several recent studies have documented a biological basis to key aspects of child social behaviour. To further explore the evolutionary basis of such differences, we investigated sex differences in sociability in wild chimpanzee, Pan troglodytes schweinfurthii, infants at Gombe National Park, Tanzania. We used a long-term data set on mother-infant behaviour to analyse the diversity of infant chimpanzee social partners from age 30 to 36 months. Male infants (N = 12) interacted with significantly more individuals than female infants did (N = 8), even when maternal sociability was controlled for. Furthermore, male infants interacted with significantly more adult males than female infants did. Our data indicate that the well-documented sex differences in adult chimpanzee social tendencies begin to appear quite early in development. Furthermore, these data suggest that the behavioural sex differences of human children are fundamentally rooted in our biological and evolutionary heritage.

When mum’s away: a study of mother and calf ego networks during separations in wild bottlenose dolphins (Tursiops sp.)

Early social development in long-lived social mammals has important implications for adult behaviour, particularly in taxa that exhibit stable long-term bonds. In one such species, bottlenose dolphins, calves have precocious locomotion, enabling them to separate from their mothers soon after birth and associate with other dolphins in the absence of direct maternal influence. To investigate mother and calf social patterns while together and separated, we analysed the ego networks of 27 mother–calf pairs constructed using group composition data from focal follows and evaluated differences based on calf sex. When separated, all calves had larger, less dense ego networks than their mothers, whereas ego networks of mother and calf when together were similar in size to those of calves, but significantly less dense. Most intriguingly, during separations, male calves’ relationships with other male calves were stronger than expected, foreshadowing the long-term bonds between adult male alliance partners. Female–female calf relationships were not stronger than expected, but when together, mothers and female calves had strong relationships with juvenile females. These results support the social bonds hypothesis and suggest that temporary separations allow calves to build and strengthen their social networks. Since bottlenose dolphins show bisexual philopatry and infant relationships can persist into adulthood, calf independence and early social development probably have implications for future success.

Kinship shapes affiliative social networks but not aggression in ring-tailed coatis

Animal groups typically contain individuals with varying degrees of genetic relatedness, and this variation in kinship has a major influence on patterns of aggression and affiliative behaviors. This link between kinship and social behavior underlies socioecological models which have been developed to explain how and why different types of animal societies evolve. We tested if kinship and age-sex class homophily in two groups of ring-tailed coatis (Nasua nasua) predicted the network structure of three different social behaviors: 1) association, 2) grooming, and 3) aggression. Each group was studied during two consecutive years, resulting in four group-years available for analysis (total of 65 individuals). Association patterns were heavily influenced by agonistic interactions which typically occurred during feeding competition. Grooming networks were shaped by mother-offspring bonds, female-female social relationships, and a strong social attraction to adult males. Mother-offspring pairs were more likely to associate and groom each other, but relatedness had no effect on patterns of aggressive behavior. Additionally, kinship had little to no effect on coalitionary support during agonistic interactions. Adult females commonly came to the aid of juveniles during fights with other group members, but females often supported juveniles who were not their offspring (57% of coalitionary interactions). These patterns did not conform to predictions from socioecological models.

Early social exposure in wild chimpanzees: mothers with sons are more gregarious than mothers with daughters.

Significance Early social experience is critical to developing appropriate adult behavior. Mothers are particularly important social partners but may also facilitate or restrict access to others. Studies investigating human parental facilitation are limited and confounded by culture. Comparative studies therefore provide invaluable insight into how parents provide social opportunities for offspring. We investigated maternal subgrouping patterns by infant sex in one of our closest relatives, chimpanzees, and found that mothers with sons were more gregarious. Infants themselves may influence patterns later in infancy, but differences were apparent early in life, when mothers and infants are in almost constant contact. Furthermore, mothers with sons associated more with adult males, potential behavioral models, early in life. These differences foreshadow sex-typical adult social behavior. In many mammals, early social experience is critical to developing species-appropriate adult behaviors. Although mother–infant interactions play an undeniably significant role in social development, other individuals in the social milieu may also influence infant outcomes. Additionally, the social skills necessary for adult success may differ between the sexes. In chimpanzees (Pan troglodytes), adult males are more gregarious than females and rely on a suite of competitive and cooperative relationships to obtain access to females. In fission–fusion species, including humans and chimpanzees, subgroup composition is labile and individuals can vary the number of individuals with whom they associate. Thus, mothers in these species have a variety of social options. In this study, we investigated whether wild chimpanzee maternal subgrouping patterns differed based on infant sex. Our results show that mothers of sons were more gregarious than mothers of daughters; differences were especially pronounced during the first 6 mo of life, when infant behavior is unlikely to influence maternal subgrouping. Furthermore, mothers with sons spent significantly more time in parties containing males during the first 6 mo. These early differences foreshadow the well-documented sex differences in adult social behavior, and maternal gregariousness may provide sons with important observational learning experiences and social exposure early in life. The presence of these patterns in chimpanzees raises questions concerning the evolutionary history of differential social exposure and its role in shaping sex-typical behavior in humans.

Chimpanzee fathers bias their behaviour towards their offspring

Promiscuous mating was traditionally thought to curtail paternal investment owing to the potential costs of providing care to unrelated infants. However, mounting evidence suggests that males in some promiscuous species can recognize offspring. In primates, evidence for paternal care exists in promiscuous Cercopithecines, but less is known about these patterns in other taxa. Here, we examine two hypotheses for paternal associations with lactating mothers in eastern chimpanzees (Pan troglodytes schweinfurthii): paternal effort, whereby males associate and interact more with their own infants, and mating effort, whereby males invest in mothers and offspring for mating privileges. We found that fathers associated more with their offspring than they did with non-kin infants, particularly early in life when infanticide risk is highest. Additionally, fathers and their infant offspring interacted more than expected. Notably, association between fathers and mother–infant pairs did not predict the probability of siring the mothers next offspring. Our results support the paternal effort, but not the mating effort hypothesis in this species. Chimpanzees are one of the most salient models for the last common ancestor between Pan and Homo, thus our results suggest that a capacity for paternal care, possibly independent of long-term mother–father bonds, existed early in hominin evolution.

Maternal Behavior by Birth Order in Wild Chimpanzees (Pan troglodytes): Increased Investment by First-Time Mothers.

Parental investment theory predicts that maternal resources are finite and allocated among offspring based on factors including maternal age and condition, and offspring sex and parity. Among humans, firstborn children are often considered to have an advantage and receive greater investment than their younger siblings. However, conflicting evidence for this “firstborn advantage” between modern and hunter-gatherer societies raises questions about the evolutionary history of differential parental investment and birth order. In contrast to humans, most nonhuman primate firstborns belong to young, inexperienced mothers and exhibit higher mortality than laterborns. In this study, we investigated differences in maternal investment and offspring outcomes based on birth order (firstborn vs. laterborn) among wild chimpanzees (Pan troglodyte schweinfurthii). During the critical first year of life, primiparous mothers nursed, groomed, and played with their infants more than did multiparous mothers. Furthermore, this pattern of increased investment in firstborns appeared to be compensatory, as probability of survival did not differ by birth order. Our study did not find evidence for a firstborn advantage as observed in modern humans but does suggest that unlike many other primates, differences in maternal behavior help afford chimpanzee firstborns an equal chance of survival.

Maternal effects on offspring stress physiology in wild chimpanzees

Early life experiences are known to influence hypothalamic‐pituitary‐adrenal (HPA) axis development, which can impact health outcomes through the individuals ability to mount appropriate physiological reactions to stressors. In primates, these early experiences are most often mediated through the mother and can include the physiological environment experienced during gestation. Here, we investigate stress physiology of dependent offspring in wild chimpanzees for the first time and examine whether differences in maternal stress physiology are related to differences in offspring stress physiology. Specifically, we explore the relationship between maternal rank and maternal fecal glucocorticoid metabolite (FGM) concentration during pregnancy and early lactation (first 6 months post‐partum) and examine whether differences based on maternal rank are associated with dependent offspring FGM concentrations. We found that low‐ranking females exhibited significantly higher FGM concentrations during pregnancy than during the first 6 months of lactation. Furthermore, during pregnancy, low‐ranking females experienced significantly higher FGM concentrations than high‐ranking females. As for dependent offspring, we found that male offspring of low‐ranking mothers experienced stronger decreases in FGM concentrations as they aged compared to males with high‐ranking mothers or their dependent female counterparts. Together, these results suggest that maternal rank and FGM concentrations experienced during gestation are related to offspring stress physiology and that this relationship is particularly pronounced in males compared to females. Importantly, this study provides the first evidence for maternal effects on the development of offspring HPA function in wild chimpanzees, which likely relates to subsequent health and fitness outcomes. Am. J. Primatol. 80:e22525, 2018.

Reproductive state and rank influence patterns of meat consumption in wild female chimpanzees (Pan troglodytes schweinfurthii).

An increase in faunivory is a consistent component of human evolutionary models. Animal matter is energy- and nutrient-dense and can provide macronutrients, minerals, and vitamins that are limited or absent in plant foods. For female humans and other omnivorous primates, faunivory may be of particular importance during the costly periods of pregnancy and early lactation. Yet, because animal prey is often monopolizable, access to fauna among group-living primates may be mediated by social factors such as rank. Wild chimpanzees (Pan troglodytes) across Africa habitually consume insects and/or vertebrates. However, no published studies have examined patterns of female chimpanzee faunivory during pregnancy and early lactation relative to non-reproductive periods, or by females of different rank. In this study, we assessed the influence of reproductive state and dominance rank on the consumption of fauna (meat and insects) by female chimpanzees of Gombe National Park, Tanzania. Using observational data collected over 38 years, we tested (a) whether faunivory varied by reproductive state, and (b) if high-ranking females spent more time consuming fauna than lower-ranking females. In single-factor models, pregnant females consumed more meat than lactating and baseline (meaning not pregnant and not in early lactation) females, and high-ranking females consumed more meat than lower-ranking females. A two-factor analysis of a subset of well-sampled females identified an interaction between rank and reproductive state: lower-ranking females consumed more meat during pregnancy than lower-ranking lactating and baseline females did. High-ranking females did not significantly differ in meat consumption between reproductive states. We found no relationships between rank or reproductive state with insectivory. We conclude that, unlike insectivory, meat consumption by female chimpanzees is mediated by both reproductive state and social rank. We outline possible mechanisms for these patterns, relate our findings to meat-eating patterns in women from well-studied hunter-gatherer societies, and discuss potential avenues for future research.