Cycle length flexibility: is the duration of sexual receptivity associated with changes in social pressures?

Research in social mammals has revealed the complexity of strategies females use in response to female-female reproductive competition and sexual conflict. One point at which competition and conflict manifests acutely is during sexual receptivity, indicated by swellings in some primates. Whether females can adjust their sexual receptivity from cycle to cycle to decrease reproductive competition and sexual conflict in response to social pressures has not been tested. As a first step, this study explores whether sexual receptivity duration is predicted by social pressures in wild female chacma baboons (Papio ursinus). Given that female baboons face intense reproductive competition and sexual coercion, we predicted that: females could shorten the duration of their sexual receptive period to reduce female-female aggression and male coercion or increase it to access multiple or their preferred male(s). We quantified 157 ovulatory cycles from 46 wild females living in central Namibia recorded over 15 years. We found no support for our hypothesis; however, our analyses revealed a negative correlation between maximal-swelling duration and group size, a proxy of within-group competition. This study provides further evidence that swelling is costly as well as a testable framework for future investigations of 'cycle length manipulation'.

Evolutionary Determinants of Nonseasonal Breeding in Wild Chacma Baboons.

AbstractAnimal reproductive phenology varies from strongly seasonal to nonseasonal, sometimes among closely related or sympatric species. While the extent of reproductive seasonality is often attributed to environmental seasonality, this fails to explain many cases of nonseasonal breeding in seasonal environments. We investigated the evolutionary determinants of nonseasonal breeding in a wild primate, the chacma baboon (Papio ursinus), living in a seasonal environment with high climatic unpredictability. We tested three hypotheses proposing that nonseasonal breeding has evolved in response to (1) climatic unpredictability, (2) reproductive competition between females favoring birth asynchrony, and (3) individual, rank-dependent variations in optimal reproductive timing. We found strong support for an effect of reproductive asynchrony modulated by rank: (i) birth synchrony is costly to subordinate females, lengthening their interbirth intervals; (ii) females alter their reproductive timings (fertility periods and conceptions) in relation to previous conceptions in the group; and (iii) the reported effect of birth synchrony on interbirth intervals weakens the intensity of reproductive seasonality at the population level. This study emphasizes the importance of sociality in mediating the evolution of reproductive phenology in group-living organisms, a result of broad significance for understanding key demographic parameters driving population responses to increasing climatic fluctuations.

Why do some primate mothers carry their infant's corpse? A cross-species comparative study.

Non-human primates respond to the death of a conspecific in diverse ways, some of which may present phylogenetic continuity with human thanatological responses. Of these responses, infant corpse carrying by mothers (ICC) is the most frequently reported. Despite its prevalence, quantitative analyses of this behaviour are scarce and inconclusive. We compiled a database of 409 published cases across 50 different primate species of mothers' responses to their infants' deaths and used Bayesian phylogenetic regressions with an information-theoretic approach to test hypotheses proposed to explain between- and within-species variation in ICC. We found that ICC was more likely when the infant's death was non-traumatic (e.g. illness) versus traumatic (e.g. infanticide), and when the mother was younger. These results support the death detection hypothesis, which proposes that ICC occurs when there are fewer contextual or sensory cues indicating death. Such an interpretation suggests that primates are able to attain an awareness of death. In addition, when carried, infant age affected ICC duration, with longer ICC observed for younger infants. This result suggests that ICC is a by-product of strong selection on maternal behaviour. The findings are discussed in the context of the evolution of emotion, and implications for evolutionary thanatology are proposed.

Developmental transitions in body color in chacma baboon infants: Implications to estimate age and developmental pace.

OBJECTIVES: In many primates, one of the most noticeable morphological developmental traits is the transition from natal fur and skin color to adult coloration. Studying the chronology and average age at such color transitions can be an easy and noninvasive method to (a) estimate the age of infants whose dates of birth were not observed, and (b) detect interindividual differences in the pace of development for infants with known birth dates. MATERIALS AND METHODS: Using a combination of photographs and field observations from 73 infant chacma baboons (Papio ursinus) of known ages, we (a) scored the skin color of six different body parts from pink to gray, as well as the color of the fur from black to gray; (b) validated our method of age estimation using photographic and field observations on an independent subset of 22 infants with known date of birth; and (c) investigated ecological, social, and individual determinants of age-related variation in skin and fur color. RESULTS: Our results show that transitions in skin color can be used to age infant chacma baboons less than 7 months old with accuracy (median number of days between actual and estimated age = 10, range = 0-86). We also reveal that food availability during the mother's pregnancy, but not during lactation, affects infant color-for-age and therefore acts as a predictor of developmental pace. DISCUSSION: This study highlights the potential of monitoring within- and between-infant variation in color to estimate age when age is unknown, and developmental pace when age is known.

Baboon thanatology: responses of filial and non-filial group members to infants' corpses.

What do animals know of death? What can animals' responses to death tell us about the evolution of species' minds, and the origins of humans' awareness of death and dying? A recent surge in interest in comparative thanatology may provide beginnings of answers to these questions. Here, we add to the comparative thanatology literature by reporting 12 cases of group members' responses to infants' deaths, including 1 miscarriage and 2 stillbirths, recorded over 13 years in wild Namibian chacma baboons. Wild baboons' responses to dead infants were similar to other primates: in general, the mother of the infant carried the infants' corpse for varying lengths of time (less than 1 h to 10 days) and tended to groom the corpses frequently, though, as in other studies, considerable individual differences were observed. However, we have not yet observed any corpse carriage of very long duration (i.e. greater than 20 days), which, though rare, occurs in other Old World monkeys and chimpanzees. We hypothesize this is due to the costs of carrying the corpse over the greater daily distances travelled by the Tsaobis baboons. Additionally, in contrast to other case reports, we observed male friends' 'protection' of the infant corpse on three occasions. We discuss the implications of these reports for current questions in the field.

Exploring individual variation in associative learning abilities through an operant conditioning task in wild baboons.

Cognitive abilities underpin many of the behavioural decisions of animals. However, we still have very little understanding of how and why cognitive abilities vary between individuals of the same species in wild populations. In this study, we assessed the associative learning abilities of wild chacma baboons (Papio ursinus) across two troops in Namibia with a simple operant conditioning task. We evaluated the ability of individuals to correctly associate a particular colour of corn kernels with a distasteful flavour through repeated presentations of two small piles of corn dyed different colours, one of which had been treated with a non-toxic bitter substance. We also assessed whether individual variation in learning ability was associated with particular phenotypic traits (sex, social rank and neophilia) and states (age and prior vigilance). We found no evidence of learning the association either within each trial or across trials, nor any variation based on individuals' phenotypes. This appeared to be due to a high tolerance for bitter foods leading to similar acceptance of both palatable and unpalatable kernels. Earlier avoidance of the bitter kernels during pilot trials suggests this higher tolerance may have been largely driven by a drought during the experiments. Overall, our findings highlight the potential influence of current environmental challenges associated with conducting cognitive tests of animals in the wild.

Insights into the evolution of social systems and species from baboon studies.

Baboons, members of the genus Papio, comprise six closely related species distributed throughout sub-Saharan Africa and southwest Arabia. The species exhibit more ecological flexibility and a wider range of social systems than many other primates. This article summarizes our current knowledge of the natural history of baboons and highlights directions for future research. We suggest that baboons can serve as a valuable model for complex evolutionary processes, such as speciation and hybridization. The evolution of baboons has been heavily shaped by climatic changes and population expansion and fragmentation in the African savanna environment, similar to the processes that acted during human evolution. With accumulating long-term data, and new data from previously understudied species, baboons are ideally suited for investigating the links between sociality, health, longevity and reproductive success. To achieve these aims, we propose a closer integration of studies at the proximate level, including functional genomics, with behavioral and ecological studies.

Correction: Women's visibility in academic seminars: Women ask fewer questions than men.

[This corrects the article DOI: 10.1371/journal.pone.0202743.].

Women's visibility in academic seminars: Women ask fewer questions than men.

The attrition of women in academic careers is a major concern, particularly in Science, Technology, Engineering, and Mathematics subjects. One factor that can contribute to the attrition is the lack of visible role models for women in academia. At early career stages, the behaviour of the local community may play a formative role in identifying ingroup role models, shaping women's impressions of whether or not they can be successful in academia. One common and formative setting to observe role models is the local departmental academic seminar, talk, or presentation. We thus quantified women's visibility through the question-asking behaviour of academics at seminars using observations and an online survey. From the survey responses of over 600 academics in 20 countries, we found that women reported asking fewer questions after seminars compared to men. This impression was supported by observational data from almost 250 seminars in 10 countries: women audience members asked absolutely and proportionally fewer questions than male audience members. When asked why they did not ask questions when they wanted to, women, more than men, endorsed internal factors (e.g., not working up the nerve). However, our observations suggest that structural factors might also play a role; when a man was the first to ask a question, or there were fewer questions, women asked proportionally fewer questions. Attempts to counteract the latter effect by manipulating the time for questions (in an effort to provoke more questions) in two departments were unsuccessful. We propose alternative recommendations for creating an environment that makes everyone feel more comfortable to ask questions, thus promoting equal visibility for women and members of other less visible groups.

Sequential phenotypic constraints on social information use in wild baboons.

Social information allows the rapid dissemination of novel information among individuals. However, an individual's ability to use information is likely to be dependent on phenotypic constraints operating at three successive steps: acquisition, application, and exploitation. We tested this novel framework by quantifying the sequential process of social information use with experimental food patches in wild baboons (Papio ursinus). We identified phenotypic constraints at each step of the information use sequence: peripheral individuals in the proximity network were less likely to acquire and apply social information, while subordinate females were less likely to exploit it successfully. Social bonds and personality also played a limiting role along the sequence. As a result of these constraints, the average individual only acquired and exploited social information on.

Phenotypic assortment in wild primate networks: implications for the dissemination of information.

Individuals' access to social information can depend on their social network. Homophily-a preference to associate with similar phenotypes-may cause assortment within social networks that could preclude information transfer from individuals who generate information to those who would benefit from acquiring it. Thus, understanding phenotypic assortment may lead to a greater understanding of the factors that could limit the transfer of information between individuals. We tested whether there was assortment in wild baboon (Papio ursinus) networks, using data collected from two troops over 6 years for six phenotypic traits-boldness, age, dominance rank, sex and the propensity to generate/exploit information-using two methods for defining a connection between individuals-time spent in proximity and grooming. Our analysis indicated that assortment was more common in grooming than proximity networks. In general, there was homophily for boldness, age, rank and the propensity to both generate and exploit information, but heterophily for sex. However, there was considerable variability both between troops and years. The patterns of homophily we observed for these phenotypes may impede information transfer between them. However, the inconsistency in the strength of assortment between troops and years suggests that the limitations to information flow may be quite variable.

Social effects on foraging behavior and success depend on local environmental conditions.

In social groups, individuals' dominance rank, social bonds, and kinship with other group members have been shown to influence their foraging behavior. However, there is growing evidence that the particular effects of these social traits may also depend on local environmental conditions. We investigated this by comparing the foraging behavior of wild chacma baboons, Papio ursinus, under natural conditions and in a field experiment where food was spatially clumped. Data were collected from 55 animals across two troops over a 5-month period, including over 900 agonistic foraging interactions and over 600 food patch visits in each condition. In both conditions, low-ranked individuals received more agonism, but this only translated into reduced foraging performances for low-ranked individuals in the high-competition experimental conditions. Our results suggest one possible reason for this pattern may be low-ranked individuals strategically investing social effort to negotiate foraging tolerance, but the rank-offsetting effect of this investment being overwhelmed in the higher-competition experimental environment. Our results also suggest that individuals may use imbalances in their social bonds to negotiate tolerance from others under a wider range of environmental conditions, but utilize the overall strength of their social bonds in more extreme environments where feeding competition is more intense. These findings highlight that behavioral tactics such as the strategic investment of social effort may allow foragers to mitigate the costs of low rank, but that the effectiveness of these tactics is likely to be limited in certain environments.

Evidence for varying social strategies across the day in chacma baboons.

Strong social bonds can make an important contribution to individual fitness, but we still have only a limited understanding of the temporal period relevant to the adjustment of social relationships. While there is growing recognition of the importance of strong bonds that persist for years, social relationships can also vary over weeks and months, suggesting that social strategies may be optimized over shorter timescales. Using biological market theory as a framework, we explore whether temporal variation in the benefits of social relationships might be sufficient to generate daily adjustments of social strategies in wild baboons. Data on grooming, one measure of social relationships, were collected from 60 chacma baboons (Papio ursinus) across two troops over a six month period. Our analyses suggest that social strategies can show diurnal variation, with subordinates preferentially grooming more dominant individuals earlier in the day compared with later in the day. These findings indicate that group-living animals may optimize certain elements of their social strategies over relatively short time periods.

Personality predicts the propensity for social learning in a wild primate.

Social learning can play a critical role in the reproduction and survival of social animals. Individual differences in the propensity for social learning are therefore likely to have important fitness consequences. We asked whether personality might underpin such individual variation in a wild population of chacma baboons (Papio ursinus). We used two field experiments in which individuals had the opportunity to learn how to solve a task from an experienced conspecific demonstrator: exploitation of a novel food and a hidden item of known food. We investigated whether the (1) time spent watching a demonstrator and (2) changes in task-solving behaviour after watching a demonstrator were related to personality. We found that both boldness and anxiety influenced individual performance in social learning. Specifically, bolder and more anxious animals were more likely to show a greater improvement in task solving after watching a demonstrator. In addition, there was also evidence that the acquisition of social information was not always correlated with its use. These findings present new insights into the costs and benefits of different personality types, and have important implications for the evolution of social learning.

Intraindividual variability of boldness is repeatable across contexts in a wild lizard.

Animals do not behave in exactly the same way when repeatedly tested in the same context or situation, even once systematic variation, such as habituation, has been controlled for. This unpredictability is called intraindividual variability (IIV) and has been little studied in animals. Here we investigated how IIV in boldness (estimated by flight initiation distances) changed across two seasons--the dry, non-breeding season and the wet, breeding season--in a wild population of the Namibian rock agama, Agama planiceps. We found significant differences in IIV both between individuals and seasons, and IIV was higher in the wet season, suggesting plasticity in IIV. Further, IIV was highly repeatable (r = 0.61) between seasons and we found strong negative correlations between consistent individual differences in flight initiation distances, i.e. their boldness, and individuals' IIVs. We suggest that to understand personality in animals, researchers should generate a personality 'profile' that includes not only the relative level of a trait (i.e. its personality), but also its plasticity and variability under natural conditions.

How do foragers decide when to leave a patch? A test of alternative models under natural and experimental conditions.

A forager's optimal patch-departure time can be predicted by the prescient marginal value theorem (pMVT), which assumes they have perfect knowledge of the environment, or by approaches such as Bayesian updating and learning rules, which avoid this assumption by allowing foragers to use recent experiences to inform their decisions. In understanding and predicting broader scale ecological patterns, individual-level mechanisms, such as patch-departure decisions, need to be fully elucidated. Unfortunately, there are few empirical studies that compare the performance of patch-departure models that assume perfect knowledge with those that do not, resulting in a limited understanding of how foragers decide when to leave a patch. We tested the patch-departure rules predicted by fixed rule, pMVT, Bayesian updating and learning models against one another, using patch residency times (PRTs) recorded from 54 chacma baboons (Papio ursinus) across two groups in natural (n = 6175 patch visits) and field experimental (n = 8569) conditions. We found greater support in the experiment for the model based on Bayesian updating rules, but greater support for the model based on the pMVT in natural foraging conditions. This suggests that foragers may place more importance on recent experiences in predictable environments, like our experiment, where these experiences provide more reliable information about future opportunities. Furthermore, the effect of a single recent foraging experience on PRTs was uniformly weak across both conditions. This suggests that foragers' perception of their environment may incorporate many previous experiences, thus approximating the perfect knowledge assumed by the pMVT. Foragers may, therefore, optimize their patch-departure decisions in line with the pMVT through the adoption of rules similar to those predicted by Bayesian updating.

Animal personality: what are behavioural ecologists measuring?

The discovery that an individual may be constrained, and even behave sub-optimally, because of its personality type has fundamental implications for understanding individual- to group-level processes. Despite recent interest in the study of animal personalities within behavioural ecology, the field is fraught with conceptual and methodological difficulties inherent in any young discipline. We review the current agreement of definitions and methods used in personality studies across taxa and systems, and find that current methods risk misclassifying traits. Fortunately, these problems have been faced before by other similar fields during their infancy, affording important opportunities to learn from past mistakes. We review the tools that were developed to overcome similar methodological problems in psychology. These tools emphasise the importance of attempting to measure animal personality traits using multiple tests and the care that needs to be taken when interpreting correlations between personality traits or their tests. Accordingly, we suggest an integrative theoretical framework that incorporates these tools to facilitate a robust and unified approach in the study of animal personality.

Exploring foraging decisions in a social primate using discrete-choice models.

There is a growing appreciation of the multiple social and nonsocial factors influencing the foraging behavior of social animals but little understanding of how these factors depend on habitat characteristics or individual traits. This partly reflects the difficulties inherent in using conventional statistical techniques to analyze multifactor, multicontext foraging decisions. Discrete-choice models provide a way to do so, and we demonstrate this by using them to investigate patch preference in a wild population of social foragers (chacma baboons Papio ursinus). Data were collected from 29 adults across two social groups, encompassing 683 foraging decisions over a 6-month period and the results interpreted using an information-theoretic approach. Baboon foraging decisions were influenced by multiple nonsocial and social factors and were often contingent on the characteristics of the habitat or individual. Differences in decision making between habitats were consistent with changes in interference-competition costs but not with changes in social-foraging benefits. Individual differences in decision making were suggestive of a trade-off between dominance rank and social capital. Our findings emphasize that taking a multifactor, multicontext approach is important to fully understand animal decision making. We also demonstrate how discrete-choice models can be used to achieve this.