Formidable females and the power trajectories of socially integrated male vervet monkeys

Sexual conflict theory expects females to avoid nonoptimal mating attempts by males. Although female vervet monkeys, Chlorocebus pygerythrus, can resist direct mating attempts, higher-ranking males still have more mating opportunities than lower-ranking ones. We presume that rank-related access reflects maleemale competition that may conflict with female reproductive objectives. We extend an earlier report of codominance in this species to show that powerful females can undermine the restrictions imposed through maleemale competition by improving the dominance rank of preferred male associates. We found that the dominance hierarchies of the sexes were comprehensively interdigitated and that males who had more female spatial associates, and who groomed with well-connected females, were more likely improve their Elo-ratings, which we use as an index of male power. The effects of partner number and integration, which predicted the probability of the initiation of aggression by lower-ranking males, suggest that association with females offered the prospect of protected threat if this likelihood increased. Although female rank and aggression were not directly consequential for males, we argue that female power and influence are intertwined and that both stem from the strength of female reproductive control

Formidable females redux: male social integration into female networks and the value of dynamic multilayer networks

The development of multilayer network techniques is a boon for researchers who wish to understand how different interaction layers might influence each other, and how these in turn might influence group dynamics. Here, we investigate how integration between male and female grooming and aggression interaction networks influences male power trajectories in vervet monkeys Chlorocebus pygerythrus. Our previous analyses of this phenomenon used a monolayer approach, and our aim here is to extend these analyses using a dynamic multilayer approach. To do so, we constructed a temporal series of male and female interaction layers. We then used a multivariate multilevel autoregression model to compare cross-lagged associations between a male’s centrality in the female grooming layer and changes in male Elo ratings. Our results confirmed our original findings: changes in male centrality within the female grooming network were weakly but positively tied to changes in their Elo ratings. However, the multilayer network approach offered additional insights into this social process, identifying how changes in a male’s centrality cascade through the other network layers. This dynamic view indicates that the changes in Elo ratings are likely to be short-lived, but that male centrality within the female network had a much stronger impact throughout the multilayer network as a whole, especially on reducing intermale aggression (i.e., aggression directed by males toward other males). We suggest that multilayer social network approaches can take advantage of increased amounts of social data that are more commonly collected these days, using a variety of methods. Such data are inherently multilevel and multilayered, and thus offer the ability to quantify more precisely the dynamics of animal social behaviors

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

Mother–offspring conflict and body temperature regulation during gestation and lactation in a wild primate

1. The physiological performance of a mother during reproduction represents a trade-off between continued investment in her current offspring, and the mother's own survival and ability to invest in future offspring. Here, we used core body temperature (Tb) patterns to examine the degree to which maternal body temperatures support the infant during periods of gestation and lactation. 2. We implanted 30 wild vervet monkeys (Chlorocebus pygerythrus) with miniature data loggers to obtain continuous measurements of core Tb during periods of typical (i.e. non-drought periods) and limited (i.e. drought period) resource availability. 3. We tracked maternal Tb profiles across the gestation and lactation periods, associated with 23 births, and compared those with Tb profiles of non-reproductive females. This allowed us to examine the flexibility in maternal body temperatures and test whether limited resource availability shifts priority away from offspring investment and towards self-maintenance. 4. Vervet monkeys demonstrated the predicted pattern of gestational hypothermia and improved homeothermy in the gestation period during typical conditions, consistent with the maintenance of a thermal gradient to facilitate heat loss from the foetus. During periods of limited resource availability (i.e. drought), mothers were less homeothermic and more hyperthermic during the gestation period. 5. Vervet monkeys showed no evidence of lactational hyperthermia during typical conditions. During the drought, lactating mothers demonstrated hyperthermia and increased variability in body temperature, consistent with the increased metabolic demands and water requirements for milk production required to support growing infants. 6. Although a mother's degree of homeothermy during gestation and lactation was unrelated to her infant's chance of survival to weaning, mothers did show flexibility in the degree to which they prioritized the maintenance of a thermal environment that supports their infant's development. Together, our findings demonstrate that flexibility in a mother's investment in thermoregulation during gestation and lactation may reflect a bet-hedging trade-off between self-maintenance and offspring investment

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 (T b) across 24 births in a population of wild vervet monkeys using biologgers. We identified distinct perturbations in T b during the birth period, including declining T b during labour and the rapid recovery of T b post-parturition. Vervet monkeys typically gave birth during their inactive phase in synchrony with the nadir of the maternal nychthemeral T b rhythm but also showed remarkable inter-individual variability in their absolute T b during birth. Our findings support the view that selection may have favoured a nocturnal timing of primate birth to coincide with lower night-time T b and environmental temperatures, which improve thermal efficiency during birth

Social integration confers thermal benefits in a gregarious primate

1. 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. 2. 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. 3. 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. 4. 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. 5. 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. 6. 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

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

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

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

Male characteristics as predictors of genital color and display variation in vervet monkeys

In the animal kingdom, conspicuous colors are often used for inter-and intra-sexual communication. Even though primates are the most colorful mammalian taxon, many questions, including what potential information color signals communicate to social partners, are not fully understood. Vervet monkeys (Chlorocebus pygerythrus) are ideal to examine the covariates of color signals. Males have multi-colored genitals, which they present during distinctive male-male interactions, known as the "Red-White-and-Blue" (RWB) display, but the genitals are also visible across a variety of other contexts, and it is unclear what this color display signals to recipients. We recorded genital color presentations and standardized digital photos of male genitals (N = 405 photos) over one mating season for 20 adult males in three groups at the Samara Private Game Reserve, South Africa. We combined these with data on male characteristics (dominance, age, tenure length, injuries, and fecal glucocorticoid metabolite concentrations). Using visual modeling methods, we measured single colors (red, white, blue) but also the contrasts between colors. We assessed the frequency of the RWB genital display and male variation in genital coloration and linked this to male characteristics. Our data suggest that the number of genital displays increased with male dominance. However, none of the variables investigated explained the inter-and intra-individual variation in male genital coloration. These results suggest that the frequency of the RWB genital display, but not its color value, is related to dominance, providing valuable insights on covariation in color signals and their display in primates. Significance statement Conspicuous colors in animals often communicate individual quality to mates and rivals. By investigating vervet monkeys, a primate species in which males present their colorful genitals within several behavioral displays, we aim to identify the covariates Communicated by E. Huchard Electronic supplementary material The online version of this article (https://doi.org/10