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Anne Pusey, Duke University

For the last 20 years, Anne has worked with the Gombe population of East African chimpanzees that was made famous by the work of Jane Goodall, and overseen the digitization of behavioral data systematically collected over the last 40 years. I currently work with Anne and colleagues to investigate the social relationships among female chimpanzees, as well as the ecological determinants of female behavior using a combination of geospatial techniques and detailed analyses of association patterns.

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Social bonds among female chimpanzees

Determinants of social preferences in female chimpanzees

Because of their low rates of affiliative interactions, there has been a long-standing debate about whether or not female chimpanzees have social bonds similar to those found in male chimpanzees and females of many other primate taxa. In addition, transient partner associations in a fission-fusion context combined with variable space use overlaps between individuals pose unique challenges for identifying true social preferences based on spatiotemporal association patterns. In recent work, I resolved these challenges by applying a new statistical approach to the largest available dataset on female chimpanzee associations. My findings provide the strongest evidence to date for the existence of active social preferences and affiliative bonds among unrelated female chimpanzees (Foerster et al., 2015). But what mediated these social choices? I found that female associations were influenced by their offspring; in particular, mothers of juvenile sons were more likely to associate with each other compared to mothers of daughters. It is likely that such preferences facilitate early social bonding among males, which may increase cooperation and future reproductive success. Further, low-ranking females appeared to bond preferentially with each other; I am currently testing whether these preferred relationships increase access to high-quality feeding habitats or reduce aggression directed at females.

Ecological constraints on chimpanzee social behavior

The distribution and abundance of food resources are among the most important factors that influence animal behavior, but also among the most difficult ones to accurately quantify. For this reason, much uncertainty still exists about how primate sociality adapts to resource constraints. Over the last two years I collaborated with Ying Zhong (Duke University) to develop models of feeding habitat quality at small spatial scales. This new method combines maximum entropy modeling of food species distributions with data on diet composition to estimate the relative importance of locations as feeding habitat (Foerster et al, in review). This method now allows me to test whether social bonds increase access to better quality habitats using long-term data on recorded feeding locations during focal animal observations. In addition to studies of small-scale determinants of social behavior within social groups, some of the most powerful insights into selective pressures on behavior can be gained by comparative studies across populations. In collaboration with Zarin Machanda (Harvard University), I aim to identify population differences in constraints on female social relationships and their potential ecological correlates. Results will greatly advance our understanding of how ecological selective pressures mediate the evolution of primate social bonds and friendships.

Health consequences of chimpanzee social bonds

Social bonds can come with potential benefits such as increased access to resources or improved health and longevity. However, they can also increase the risk of pathogen transmission. The outcome of this tradeoff might critically influence the evolution of sociality, yet remains poorly understood. Collaborating with Thomas Gillespie (Emory University) and colleagues I tested whether chimpanzee social contact facilitates the transmission of gastrointestinal parasites, as suggested by recent studies on other species. Results show that more gregarious individuals (those who spend more time in larger subgroups) have more parasites and that, all else being equal, individuals with stronger grooming bonds have fewer parasites (Foerster et al., in prep.). These findings suggest that there is a measurable health benefit to social bonds and that an optimal social strategy may consist of minimizing gregariousness while maintaining strong grooming bonds. I found further support for the beneficial effects of social contact through a collaboration with Andrew Moeller (Yale University) and colleagues, which indicated that stronger social connections contribute to the maintenance of shared gut microbial communities, and possibly the evolution of adaptive microbiome composition within and between chimpanzee host generations (Moeller, Foerster, et al., accepted). Given research in other study systems on the interaction between gut microbiota and intestinal parasites, future work could test whether the sharing of adaptive microbial communities through social contact helps limit parasitic infections.

  • Eastern chimpanzee feeding on vines in Gombe National Park, Tanzania

Habitat quality and its influence on chimpanzee behavior

The distribution and abundance of food resources are among the most important factors that influence animal behavioral strategies. Yet, spatial variation in feeding habitat quality is often difficult to assess with traditional methods that rely on extrapolation from plot survey data or remote sensing. In a manuscript currently in press in Behavioral Ecology, I show that maximum entropy species distribution modeling can be used to successfully predict small-scale variation in the distribution of 24 important plant food species for chimpanzees at Gombe National Park, Tanzania. The level of resolution is 10 meters, and the predictive accuracy of species distributions ranges between 70-95%, with most species lying above 80%. Combined with behavioral observations on what food is being selected in any given time period, the predicted species distributions allow the assessment of feeding habitat quality as the cumulative dietary proportion of the species predicted to occur in a given location. This measure exhibits considerable spatial heterogeneity with elevation and latitude at Gombe, both within and across main habitat types. This illustrates that reliance on broad habitat types can mask important determinants of behavior.

I have begun to use this new measure of habitat quality to gain insights into the ecological correlates of chimpanzee behavior. In a first analysis, I assessed individual variation in habitat selection among adult chimpanzees during a ten-year period, testing predictions about tradeoffs between foraging and reproductive effort. I found that non-swollen females selected the highest quality habitats compared to swollen females or males, in line with predictions based on their energetic needs. Swollen females appeared to compromise feeding in favor of mating opportunities, suggesting that females rather than males change their ranging patterns in search of mates. Males generally occupied feeding habitats of lower quality, which may exacerbate energetic challenges of aggression and territory defense. Finally, I documented an increase in feeding habitat quality with community residence time in both sexes, suggesting an influence of familiarity on foraging decisions in a highly heterogeneous landscape.

Human social development

Efe

photo by Paula Ivey-Henry

The study of early social development can provide useful insights into the psychological and biological adaptations to human sociality. Unfortunately, modern cultural influences on child-rearing practices are not necessarily adaptive and provide only limited insights into the developmental processes that interact with adult human social behavior and social structure. Together with Gilda Morelli (Boston College) and Paula Ivey-Henry (Harvard School of Public Health), I investigated the social development of Efe hunter-gatherers in Central Africa. Our analyses uncovered extensive early social integration of infants and toddlers beyond levels previously reported in other human societies. Interestingly, this early social integration occurred in an ecological context that constrains maternal investment and enforces strong dependency on others, indicating the adaptive value of early social bonding in human fission-fusion societies.

This work has thus far been published in an edited volume on the “Ancestral landscapes in human evolution“. Please click here for a PDF version of the chapter, and here for a published commentary. A recent review of the book provides further context and is available here.

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Ying Zhong

Ying is a second-year Masters student in the Nicholas School of the Environment’s at Duke University. She is working on a project to predict the distribution of important chimpanzee food species at Gombe National Park, Tanzania, using state-of-the-art species distribution models in combination with spatial information on feeding behavior recorded from focal observations. Her work will help us develop a detailed chimpanzee habitat quality surface for Gombe, which offers new and exciting opportunities to answer questions about the adaptive value of chimpanzee behavior and ecology. Ying’s career interests lie in landscape ecology and geospatial analyses, which she hopes to pursue in the context of a research institute or conservation organization in the coming years.

  • Chandra Swanson

Chandra Swanson

Chandra is a senior undergraduate student at Duke University, majoring in Evolutionary Anthropology and Global Health. She currently conducts senior thesis research quantifying female reproductive health among chacma baboons from the Tokai Baboon Sociality Project, using both hormonal and observational indicators of reproductive function. She will test multiple hypotheses about the determinants of individual variation in reproductive health measures, assess whether fecal hormone metabolites can be used to detect early fetal loss, and collaborate with another project to assess the relationship between parasite infection levels and reproductive health.

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Anna Willoughby

Anna is a senior undergraduate student at Duke University, and conducting her thesis research on parasite-host dynamics in female chacma baboons of the Tokai Baboon Sociality Project. In particular, she is interested in the determinants of individual variation in infection risk and infection intensities with common intestinal helminth taxa, which she examines using a combination of hormonal indicators of energy balance and physiological stress responses. A second focus of her work is the little understood association between parasite infections and behavioral changes that influence parasite-host dynamics.  Her work contributes to the larger question of how changes in individual behavior influence health and reproductive performance, in the context of natural social groups of non-human primates.

Project Overview

IMG_7570In many primate societies, individuals form strong, long-lasting social bonds. It is now known that these bonds can be adaptive, for example by increasing longevity, offspring survival, and, ultimately, reproductive success. What is still poorly understood are the mechanisms by which social bonds achieve their effects. One possibility is that because of their known function in helping individuals cope with stressors, social bonds mitigate negative effects of chronic stress on health and reproduction. But whether – and how – social stress in wild social groups of primates influences female reproduction is also poorly understood.

The Tokai Baboon Sociality Project addresses these gaps in our knowledge by testing three potential pathways that could connect variation in social bonds with measures of health and reproductive function: 1) the lack of strong social bonds leads to elevated stress hormone levels that in turn mediate increased susceptibility to intestinal parasite infections, with potential effects on energy availability; 2) social stress influences reproductive physiology directly; 3) social bonds mediate success in feeding competition; and 4) social bonds (particularly with males) reduce exposure to aggression and infanticide risk.

Foerster-2014-001-IMG_7627Data for this project are currently being collected from two troops of chacma baboons (Papio ursinus) on the Cape Peninsula of South Africa. Methods include (1) behavioral observations to document sources of stress and social bonds; (2) measurement of stress and reproductive hormone levels in fecal samples; (3) examination of intestinal parasites from fecal samples; (4) measurement of energy balance via urinary C-peptide, a byproduct of insulin production; and (5) a novel field experiment in which intestinal parasites are eliminated from a random selection of females to assess, for the first time in a wild primate, the factors associated with the timing and intensity of re-infection.

Ultimately, this project will generate new insights into the mechanisms linking social behavior, stress physiology, health, and reproduction and help elucidate the function of social bonds in primate societies. Because baboons share many traits with humans and are useful in studying aspects of human biology, this project will both help us understand the benefits of sociality during human evolution and carry clinical implications by elucidating the role of social stress as a risk factor for parasite infections.

Background

Foerster-2014-001-IMG_7861Glucocorticoids or GCs (stress hormones) such as cortisol are the primary mediators of physiological responses to physical or psychological perturbations from homeostasis in all vertebrates. During acute stress responses, these hormones optimize the availability of energy needed to cope with a stressor and activate important aspects of the immune system. When exposure to a stressor exceeds the coping capacity of the organism, however, the beneficial actions of stress hormones turn into maladaptive responses that contribute to the depletion of bodily resources, increase disease risk and progression, and may even lead to death.

20140209_061240Non-invasive techniques to quantify GC metabolites in urine or feces have resulted in a growing number of studies that use GCs to assess “costly” aspects of behavior and life history in wild vertebrates. The interpretation of naturally occurring hormonal variation is rendered difficult, however, by the dearth of studies documenting effects of variable stress levels on reproduction in non-human primates and humans. Much of what we know about the health effects of social stress comes from studies conducted on captive non-human primates, or from modern human societies where natural social coping mechanisms may be impaired and individuals subject to high levels of life and work stress. Given its partly adaptive function, some observed variation in stress levels is likely tied to fitness-maximizing strategies; this may explain why a recent review of vertebrate studies found conflicting evidence for a relationship between GCs and indicators of fitness.

TK1600_P1120543o interpret stress responses in wild primates using non-invasive measures and to understand their evolutionary significance, it is necessary to (a) study tangible fitness correlates and how they are modulated by, or modulate, GCs, (b) collect longitudinal data on individual stress responses and measures of reproductive function, (c) study free-ranging populations, because artificially high levels of psychological stress that often occur in captivity are unlikely to reflect daily life experiences in an evolutionary context, and (d) disentangle the influence of social stressors from that of energetic stressors.

The Tokai Baboon Project tries to meet these requirements by (1) studying social groups that are free-ranging but relatively well buffered against energetic stressors due to partial reliance on anthropogenic food sources; (2) collecting a large number of biological samples to arrive at representative estimates of hormone metabolites; (3) evaluating multiple potential stressors and controlling for confounds of stress responses using modern statistical tools, and (4) quantifying the association of GC variation with two potential fitness correlates: reproductive function and the number and relative intensity of gastro-intestinal (GIT) parasite infections. GIT parasite infections are a potential correlate of fitness because they can have effects on host nutrition, immunology, and reproduction, and are known to influence health and morbidity in humans.