Estimates of life history parameters in a high latitude, arid-country vervet monkey population.

We present data on life history parameters from a long-term study of vervet monkeys in the Eastern Cape, South Africa. Estimates are presented of age at first conception for females and age at natal dispersal for males, along with the probability of survival to adulthood for infants born during the study, female reproductive life-span, reproductive output (including lifetime reproductive success for a subset of females), and inter-birth interval (IBI) duration. We also assess the effect of maternal age and infant survival on length of IBI. We then go on to compare life history parameters for our population with those from two East African populations in Kenya (Amboseli and Laikipia). We find there is broad consensus across the three populations, although mean infant survival was considerably lower for the two East African sites. Such comparisons must be made cautiously, however, as local ecology across the duration of the studies obviously has an impact on the estimates obtained. With this caveat in place, we consider that the concordance between values is sufficient to enable the values reported here to be used in comparative studies of primate life history, although data from habitats with higher rainfall and lower levels of seasonality are needed, and the results presented here should not be seen as canonical.

Using network synchrony to identify drivers of social dynamics.

Social animals frequently show dynamic social network patterns, the consequences of which are felt at the individual and group level. It is often difficult, however, to identify what drivers are responsible for changes in these networks. We suggest that patterns of network synchronization across multiple social groups can be used to better understand the relative contributions of extrinsic and intrinsic drivers. When groups are socially separated, but share similar physical environments, the extent to which network measures across multiple groups covary (i.e. network synchrony) can provide an estimate of the relative roles of extrinsic and intrinsic drivers. As a case example, we use allogrooming data from three adjacent vervet monkey groups to generate dynamic social networks. We found that network strength was strongly synchronized across the three groups, pointing to shared extrinsic environmental conditions as the driver. We also found low to moderate levels of synchrony in network modularity, suggesting that intrinsic social processes may be more important in driving changes in subgroup formation in this population. We conclude that patterns of network synchronization can help guide future research in identifying the proximate mechanisms behind observed social dynamics in animal groups.

The thermal consequences of primate birth hour and its evolutionary implications.

Most primates, including humans, give birth during the inactive phase of the daily cycle. Practical constraints therefore limit our knowledge of the precise timing of nocturnal birth in wild diurnal primates and so limit our understanding of selective pressures and consequences. We measured maternal core body temperature (Tb) across 24 births in a population of wild vervet monkeys using biologgers. We identified distinct perturbations in Tb during the birth period, including declining Tb during labour and the rapid recovery of Tb post-parturition. Vervet monkeys typically gave birth during their inactive phase in synchrony with the nadir of the maternal nychthemeral Tb rhythm but also showed remarkable inter-individual variability in their absolute Tb during birth. Our findings support the view that selection may have favoured a nocturnal timing of primate birth to coincide with lower night-time Tb and environmental temperatures, which improve thermal efficiency during birth.

Experts in action: why we need an embodied social brain hypothesis.

The anthropoid primates are known for their intense sociality and large brain size. The idea that these might be causally related has given rise to a large body of work testing the 'social brain hypothesis'. Here, the emphasis has been placed on the political demands of social life, and the cognitive skills that would enable animals to track the machinations of other minds in metarepresentational ways. It seems to us that this position risks losing touch with the fact that brains primarily evolved to enable the control of action, which in turn leads us to downplay or neglect the importance of the physical body in a material world full of bodies and other objects. As an alternative, we offer a view of primate brain and social evolution that is grounded in the body and action, rather than minds and metarepresentation. This article is part of the theme issue 'Systems neuroscience through the lens of evolutionary theory'.

Fevers and the social costs of acute infection in wild vervet monkeys.

Fevers are considered an adaptive response by the host to infection. For gregarious animals, however, fever and the associated sickness behaviors may signal a temporary loss of capacity, offering other group members competitive opportunities. We implanted wild vervet monkeys (Chlorocebus pygerythrus) with miniature data loggers to obtain continuous measurements of core body temperature. We detected 128 fevers in 43 monkeys, totaling 776 fever-days over a 6-year period. Fevers were characterized by a persistent elevation in mean and minimum 24-h body temperature of at least 0.5 °C. Corresponding behavioral data indicated that febrile monkeys spent more time resting and less time feeding, consistent with the known sickness behaviors of lethargy and anorexia, respectively. We found no evidence that fevers influenced the time individuals spent socializing with conspecifics, suggesting social transmission of infection within a group is likely. Notably, febrile monkeys were targeted with twice as much aggression from their conspecifics and were six times more likely to become injured compared to afebrile monkeys. Our results suggest that sickness behavior, together with its agonistic consequences, can carry meaningful costs for highly gregarious mammals. The degree to which social factors modulate the welfare of infected animals is an important aspect to consider when attempting to understand the ecological implications of disease.

Tolerance of muzzle contact underpins the acquisition of foraging information in vervet monkeys (Chlorocebus pygerythrus).

Muzzle contact, where one animal brings its muzzle into close proximity to that of another, has often been hypothesized as a straightforward means of socially mediated food investigation. Using 2,707 observations of muzzle contact occurring across 3 troops of wild vervet monkeys (Chlorocebus pygerythrus), we tested this social learning hypothesis. We first explored the social structuring of muzzle contact by analyzing the characteristics of initiators and receivers. Similar to previous research, juveniles initiated contact at higher rates than adults, particularly toward adult females and animals with lower dominance rankings. The highest number of contacts occurred between kin compared to contacts between nonkin. However, on the whole, contacts occurred at low rates, even among kin dyads. We next determined whether muzzle contact was used as a means to learn socially, specifically by animals seeking foraging information. We found that initiators did not overwhelmingly target foragers, meaning animals do not appear to directly seek information about food during muzzle contact. However, animals that contacted foragers were more likely forage themselves in comparison to those that contacted nonforagers, suggesting that foragers do provide food information. These findings indicate that both kin and low-ranking animals serve as discriminative stimuli for social tolerance and that foraging animals serve as discriminative stimuli for food availability. We conclude that broad social tolerance, rather than the recipient's knowledge, is the most likely antecedent to muzzle contact and that animals engage in this behavior as a low-cost means of maintaining a baseline level of information about their environment. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Field data confirm the ability of a biophysical model to predict wild primate body temperature.

In the face of climate change there is an urgent need to understand how animal performance is affected by environmental conditions. Biophysical models that use principles of heat and mass transfer can be used to explore how an animal's morphology, physiology, and behavior interact with its environment in terms of energy, mass and water balances to affect fitness and performance. We used Niche Mapper™ (NM) to build a vervet monkey (Chlorocebus pygerythrus) biophysical model and tested the model's ability to predict core body temperature (Tb) variation and thermal stress against Tb and behavioral data collected from wild vervets in South Africa. The mean observed Tb in both males and females was within 0.5 °C of NM's predicted Tbs for 91% of hours over the five-year study period. This is the first time that NM's Tb predictions have been validated against field data from a wild endotherm. Overall, these results provide confidence that NM can accurately predict thermal stress and can be used to provide insight into the thermoregulatory consequences of morphological (e.g., body size, shape, fur depth), physiological (e.g. Tb plasticity) and behavioral (e.g., huddling, resting, shade seeking) adaptations. Such an approach allows users to test hypotheses about how animals adapt to thermoregulatory challenges and make informed predictions about potential responses to environmental change such as climate change or habitat conversion. Importantly, NM's animal submodel is a general model that can be adapted to other species, requiring only basic information on an animal's morphology, physiology and behavior.

Infrared thermography cannot be used to approximate core body temperature in wild primates.

Understanding the physiological processes that underpin primate performance is key if we are to assess how a primate might respond when navigating new and changing environments. Given the connection between a mammal's ability to thermoregulate and the changing demands of its thermal environment, increasing attention is being devoted to the study of thermoregulatory processes as a means to assess primate performance. Infrared thermography can be used to record the body surface temperatures of free-ranging animals. However, some uncertainty remains as to how these measurements can be used to approximate core body temperature. Here, we use data collected from wild vervet monkeys (Chlorocebus pygerythrus) to examine the relationship between infrared body surface temperature, core body (intra-abdominal) temperature, and local climate, to determine to what extent surface temperatures reflect core body temperature. While we report a positive association between surface and core body temperature-a finding that has previously been used to justify the use of surface temperature measurements as a proxy for core temperature regulation-when we controlled for the effect of the local climate in our analyses, this relationship was no longer observed. That is, body surface temperatures were solely predicted by local climate, and not core body temperatures, suggesting that surface temperatures tell us more about the environment a primate is in, and less about the thermal status of its body core in that environment. Despite the advantages of a noninvasive means to detect and record animal temperatures, infrared thermography alone cannot be used to approximate core body temperature in wild primates.

Climate induced stress and mortality in vervet monkeys.

As the effects of global climate change become more apparent, animal species will become increasingly affected by extreme climate and its effect on the environment. There is a pressing need to understand animal physiological and behavioural responses to climatic stressors. We used the reactive scope model as a framework to investigate the influence of drought conditions on vervet monkey (Chlorocebus pygerythrus) behaviour, physiological stress and survival across 2.5 years in South Africa. Data were collected on climatic, environmental and behavioural variables and physiological stress via faecal glucocorticoid metabolites (fGCMs). There was a meaningful interaction between water availability and resource abundance: when food availability was high but standing water was unavailable, fGCM concentrations were higher compared to when food was abundant and water was available. Vervet monkeys adapted their behaviour during a drought period by spending a greater proportion of time resting at the expense of feeding, moving and social behaviour. As food availability decreased, vervet mortality increased. Peak mortality occurred when food availability was at its lowest and there was no standing water. A survival analysis revealed that higher fGCM concentrations were associated with an increased probability of mortality. Our results suggest that with continued climate change, the increasing prevalence of drought will negatively affect vervet abundance and distribution in our population. Our study contributes to knowledge of the limits and scope of behavioural and physiological plasticity among vervet monkeys in the face of rapid environmental change.

Gastrointestinal Parasites of Vervet Monkeys (Chlorocebus pygerythrus) in a High Latitude, Semi-Arid Region of South Africa.

Given a changing climate and large-scale human migration, understanding infectious diseases in wildlife and the factors that drive the spread of these diseases is becoming increasingly important. Owing to the close phylogenetic relationship between nonhuman primates and humans, primate parasites are of particular interest due to the potential for zoonotic disease transmission and for the study of social transmission within gregarious social groups. There is a wide range of social and environmental factors that influence the prevalence and transmission of pathogens, and identifying these, and their effects, is crucial to understanding the population-level consequences of climate change for animals that live in obligate social groups. Here we investigated gastrointestinal parasite species richness and used fecal egg counts to estimate worm intensities in 3 vervet monkey troops (Chlorocebus pygerythrus) in a high latitude, semi-arid region of South Africa. This region is characterized by unpredictable rainfall and temperature extremes in summer and winter. We identified the gastrointestinal parasites in the population and explored potential demographic predictors, namely sex and troop membership, of parasite species richness and estimated intensity. Additionally, we assessed whether there was short-term intra-individual, inter-sample consistency in egg counts. Six species of gastrointestinal helminths were identified from 3 study troops, with egg counts ranging from 0 eggs/g to 1,100 eggs/g. Neither age nor sex predicted species richness or estimated intensity. This population had the highest prevalence of parasites with an insect vector compared with all other vervet populations studied, and distinctively high prevalences of Trichostrongylus sp. (71%) and Ternidens sp. (27%). Additionally, we found intra-individual egg count consistency in the short term (mean: 32 days).

Functional social structure in baboons: Modeling interactions between social and environmental structure in group-level foraging.

In mobile social groups, cohesion is thought to be driven by patterns of attraction at both the individual and group level. In long-lived species with high group stability and repeated interactions, such as baboons, individual-to-individual attractions have the potential to play a large role in group cohesion and overall movement patterns. In previous work, we found that the patterning of inter-individual attraction gave rise to an emergent group-level structure, whereby a core of more influential, inter-dependent individuals exerted a unidirectional influence on the movements of peripheral animals. Here, we use agent-based modeling of baboon groups to investigate whether this core-periphery structure has any functional consequences for foraging behavior. By varying individual level attractions, we produced baboon groups that contained influence structures that varied from more to less centralized. Our results suggest that varying centrality affects both the ability of the group to detect resource structure in the environment, as well as the ability of the group to exploit these resources. Our models predict that foraging groups with more centralized social structures will show a reduction in detection and an increase in exploitation of resources in their environment, and will produce more extreme foraging outcomes. More generally, our results highlight how a group's internal social structure can result in mobile social animals being able to more (or less) effectively exploit environmental structure, and capitalize on the distribution of resources. In addition, our agent-based model can be used to generate testable predictions that can be tested among the extant baboon allotaxa. This will add value to the existing body of work on responses to local ecology, as well as providing a means to test hypotheses relating to the phylogeography of the baboons and, by analogy, shed light on patterns of hominin evolution in time and space.

Assessment of Male Reproductive Skew via Highly Polymorphic STR Markers in Wild Vervet Monkeys, Chlorocebus pygerythrus.

Male reproductive strategies have been well studied in primate species where the ability of males to monopolize reproductive access is high. Less is known about species where males cannot monopolize mating access. Vervet monkeys (Chlorocebus pygerythrus) are interesting in this regard as female codominance reduces the potential for male monopolization. Under this condition, we assessed whether male dominance rank still influences male mating and reproductive success, by assigning paternities to infants in a population of wild vervets in the Eastern Cape, South Africa. To determine paternity, we established microsatellite markers from noninvasive fecal samples via cross-species amplification. In addition, we evaluated male mating and reproductive success for 3 groups over 4 mating seasons. We identified 21 highly polymorphic microsatellites (number of alleles = 7.5 ± 3.1 [mean ± SD], observed heterozygosity = 0.691 ± 0.138 [mean ± SD]) and assigned paternity to 94 of 97 sampled infants (96.9%) with high confidence. Matings pooled over 4 seasons were significantly skewed across 3 groups, although skew indices were low (B index = 0.023-0.030) and mating success did not correlate with male dominance. Paternities pooled over 4 seasons were not consistently significantly skewed (B index = 0.005-0.062), with high-ranking males siring more offspring than subordinates only in some seasons. We detected 6 cases of extra-group paternity (6.4%) and 4 cases of natal breeding (4.3%). Our results suggest that alternative reproductive strategies besides priority of access for dominant males are likely to affect paternity success, warranting further investigation into the determinants of paternity among species with limited male monopolization potential.

Network integration and limits to social inheritance in vervet monkeys.

Social networks can be adaptive for members and a recent model (Ilany and Akçay 2016 Nat. Comm.7, 12084 (doi:10.1038/ncomms12084)) has demonstrated that network structure can be maintained by a simple process of social inheritance. Here, we ask how juvenile vervet monkeys integrate into their adult grooming networks, using the model to test whether observed grooming patterns replicate network structure. Female juveniles, who are philopatric, increased their grooming effort towards adults more than males, although this was not reciprocated by the adults themselves. While more consistent maternal grooming networks, together with maternal network strength, predicted increasing similarity in the patterning of mother-daughter grooming allocations, daughters' grooming networks generally did not match closely those of their mothers. However, maternal networks themselves were not very consistent across time, thus presenting youngsters with a moving target that may be difficult to match. Observed patterns of juvenile female grooming did not replicate the adult network, for which increased association with adults not groomed by their mothers would be necessary. These results suggest that network flexibility, not stability, characterizes our groups and that juveniles are exposed to, and must learn to cope with, temporal shifts in network structure. We hypothesize that this may lead to individual variation in behavioural flexibility, which in turn may help explain why and how variation in sociability influences fitness.

Faecal glucocorticoid metabolite monitoring as a measure of physiological stress in captive and wild vervet monkeys.

The development of non-invasive techniques to analyse physiological stress in mammalian species has revolutionised field-based endocrinology. However, careful validation of the methods used to determine faecal glucocorticoid metabolite (fGCM) and other hormone concentrations are required on a species- and sex-specific basis. In this study, we performed an adrenocorticotropic hormone (ACTH) stimulation test on four (two male and two female) captive vervet monkeys (Chlorocebus pygerythrus) to determine the most appropriate enzyme immunoassay (EIA) from a suite of available EIAs. Furthermore, we took advantage of a potentially stressful event in our wild vervet population from Samara Private Game Reserve, South Africa, to examine if an alpha-beta female rank reversal increases the physiological stress of those individuals directly involved, as well as other group members. Both our physiological and biological validation studies revealed that a cortisol assay was the most appropriate EIA for monitoring fGCM alterations in vervet monkeys. In addition, we found that the observed rank-reversal had no significant effect on the physiological stress levels of uninvolved group members. Our study highlights that physiological validation is imperative and, where possible, should be conducted in parallel with a carefully considered biologically-relevant test under natural conditions. Overall, our results provide a necessary step for future studies to examine physiological stress of vervet monkeys via fGCM monitoring by validating a suitable EIA for this species. This paves the way for future research into the health and welfare of both captive and wild vervet monkeys, and will allow researchers to assess the behavioural, social and ecological correlates of physiological stress levels of this species.

Individual-level movement bias leads to the formation of higher-order social structure in a mobile group of baboons.

In mobile social groups, influence patterns driving group movement can vary between democratic and despotic. The arrival at any single pattern of influence is thought to be underpinned by both environmental factors and group composition. To identify the specific patterns of influence driving travel decision-making in a chacma baboon troop, we used spatially explicit data to extract patterns of individual movement bias. We scaled these estimates of individual-level bias to the level of the group by constructing an influence network and assessing its emergent structural properties. Our results indicate that there is heterogeneity in movement bias: individual animals respond consistently to particular group members, and higher-ranking animals are more likely to influence the movement of others. This heterogeneity resulted in a group-level network structure that consisted of a single core and two outer shells. Here, the presence of a core suggests that a set of highly interdependent animals drove routine group movements. These results suggest that heterogeneity at the individual level can lead to group-level influence structures, and that movement patterns in mobile social groups can add to the exploration of both how these structures develop (i.e. mechanistic aspects) and what consequences they have for individual- and group-level outcomes (i.e. functional aspects).

Thermal consequences of increased pelt loft infer an additional utilitarian function for grooming.

A strong case has been made that the primary function of grooming is hygienic. Nevertheless, its persistence in the absence of hygienic demand, and its obvious tactical importance to members of primate groups, underpins the view that grooming has become uncoupled from its utilitarian objectives and is now principally of social benefit. We identify improved thermoregulatory function as a previously unexplored benefit of grooming and so broaden our understanding of the utilitarian function of this behavior. Deriving the maximum thermal benefits from the pelt requires that it be kept clean and that the loft of the pelt is maintained (i.e., greater pelt depth), both of which can be achieved by grooming. In a series of wind-tunnel experiments, we measured the heat transfer characteristics of vervet monkey (Chlorocebus pygerythrus) pelts in the presence and absence of backcombing, which we used as a proxy for grooming. Our data indicate that backcombed pelts have improved thermal performance, offering significantly better insulation than flattened pelts and, hence, better protection from the cold. Backcombed pelts also had significantly lower radiant heat loads compared to flattened pelts, providing improved protection from radiant heat. Such thermal benefits, therefore, furnish grooming with an additional practical value to which its social use is anchored. Given the link between thermoregulatory ability and energy expenditure, our findings suggest that grooming for thermal benefits may be an important explanatory variable in the relationship between levels of sociability and individual fitness. Am. J. Primatol. 78:456-461, 2016. © 2015 Wiley Periodicals, Inc.

Taking the aggravation out of data aggregation: A conceptual guide to dealing with statistical issues related to the pooling of individual-level observational data.

Field data often include multiple observations taken from the same individual. In order to avoid pseudoreplication, it is commonplace to aggregate data, generating a mean score per individual, and then using these aggregated data in subsequent analyses. Aggregation, however, can generate problems of its own. Not only does it lead to a loss of information, it can also leave analyses vulnerable to the "ecological fallacy": the drawing of false inferences about individual behavior on the basis of population level ("ecological") data. It can also result in Simpson's paradox, where relationships seen at the individual level can be completely reversed when analyzed at the aggregate level. These phenomena have been documented widely in the medical and social sciences but tend to go unremarked in primatological studies that rely on observational data from the field. Here, we provide a conceptual guide that explains how and why aggregate data are vulnerable to the ecological fallacy and Simpson's paradox, illustrating these points using data on baboons. We then discuss one particular analytical approach, namely multi-level modeling, that can potentially eliminate these problems. By highlighting the issue of the ecological fallacy, and increasing awareness of how datasets are often organized into a number of different levels, we also highlight the manner in which researchers can more positively exploit the structure of their datasets, without any information loss. These analytical approaches may thus provide greater insight into behavior by permitting more thorough investigation of interactions and cross-level effects.

Social integration confers thermal benefits in a gregarious primate.

Sociality has been shown to have adaptive value for gregarious species, with more socially integrated animals within groups experiencing higher reproductive success and longevity. The value of social integration is often suggested to derive from an improved ability to deal with social stress within a group; other potential stressors have received less attention. We investigated the relationship between environmental temperature, an important non-social stressor, and social integration in wild female vervet monkeys (Chlorocebus pygerythrus), using implanted data loggers to obtain direct measures of core body temperature. Heterothermy (as measured by 24-h amplitude of body temperature) increased, and 24-h minima of body temperature decreased, as the 24-h minimum ambient temperature decreased. As winter progressed, monkeys became increasingly heterothermic and displayed lower 24-h minima of body temperature. Monkeys with a greater number of social partners displayed a smaller 24-h amplitude (that is, were more homoeothermic) and higher 24-h minima of body temperature (that is, became less hypothermic), than did animals with fewer social partners. Our findings demonstrate that social integration has a direct influence on thermoregulatory ability: individual animals that form and maintain more social relationships within their group experience improved thermal competence compared to those with fewer social relationships. Given the likely energetic consequences of thermal benefits, our findings offer a viable physiological explanation that can help account for variations in fitness in relation to individual differences in social integration.

Behavioral flexibility of vervet monkeys in response to climatic and social variability.

Responses to environmental variability sheds light on how individuals are able to survive in a particular habitat and provides an indication of the scope and limits of its niche. To understand whether climate has a direct impact on activity, and determine whether vervet monkeys have the behavioral flexibility to respond to environmental change, we examined whether the amount of time spent resting and feeding in the nonmating and mating seasons were predicted by the thermal and energetic constraints of ambient temperature. Our results show that high temperatures during the nonmating season were associated with an increase in time spent resting, at the expense of feeding. Cold temperatures during the nonmating season were associated with an increase in time spent feeding, at the expense of resting. In contrast, both feeding and resting time during the mating season were independent of temperature, suggesting that animals were not adjusting their activity in relation to temperature during this period. Our data indicate that climate has a direct effect on animal activity, and that animals may be thermally and energetically compromised in the mating season. Our study animals appear to have the behavioral flexibility to tolerate current environmental variability. However, future climate change scenarios predict that the time an animal has available for behaviors critical for survival will be constrained by temperature. Further investigations, aimed at determining the degree of behavioral and physiological flexibility displayed by primates, are needed if we are to fully understand the consequences of environmental change on their distribution and survival.

Ontogenetic scaling of fore- and hind limb posture in wild chacma baboons (Papio hamadryas ursinus).

Large-scale interspecific studies of mammals ranging between 0.04-280 kg have shown that larger animals walk with more extended limb joints. Within a taxon or clade, however, the relationship between body size and joint posture is less straightforward. Factors that may affect the lack of congruence between broad and narrow phylogenetic analyses of limb kinematics include limited sampling of (1) ranges of body size, and/or (2) numbers of individuals. Unfortunately, both issues are inherent in laboratory-based or zoo locomotion research. In this study, we examined the relationship between body mass and elbow and knee joint angles (our proxies of fore- and hind limb posture, respectively) in a cross-sectional ontogenetic sample of wild chacma baboons (Papio hamadryas ursinus) habituated in the De Hoop Nature Reserve, South Africa. Videos were obtained from 33 individuals of known age (12 to ≥ 108 months) and body mass (2-29.5 kg) during walking trials. Results show that older, heavier baboons walk with significantly more extended knee joints but not elbow joints. This pattern is consistent when examining only males, but not within the female sample. Heavier, older baboons also display significantly less variation in their hind limb posture compared to lighter, young animals. Thus, within this ontogenetic sample of a single primate species spanning an order of magnitude in body mass, hind limb posture exhibited a postural scaling phenomenon while the forelimbs did not. These findings may further help explain 1) why younger mammals (including baboons) tend to have relatively stronger bones than adults, and 2) why humeri appear relatively weaker than femora (in at least baboons). Finally, this study demonstrates how field-acquired kinematics can help answer fundamental biomechanical questions usually addressed only in animal gait laboratories.