Determinants of immigration strategies in male crested macaques (Macaca nigra).

Immigration into a new group can produce substantial costs due to resistance from residents, but also reproductive benefits. Whether or not individuals base their immigration strategy on prospective costbenefit ratios remains unknown. We investigated individual immigration decisions in crested macaques, a primate species with a high reproductive skew in favour of high-ranking males. We found two different strategies. Males who achieved low rank in the new group usually immigrated after another male had immigrated within the previous 25 days and achieved high rank. They never got injured but also had low prospective reproductive success. We assume that these males benefitted from immigrating into a destabilized male hierarchy. Males who achieved high rank in the new group usually immigrated independent of previous immigrations. They recieved injuries more frequently and therefore bore immigration costs. They, however, also had higher reproductive success prospects. We conclude that male crested macaques base their immigration strategy on relative fighting ability and thus potential rank in the new group i.e. potential reproductive benefits, as well as potential costs of injury

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

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

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

Mate-guarding constrains feeding activity but not energetic status of wild male long-tailed macaques (Macaca fascicularis).

Mate-guarding is an important determinant of male reproductive success in a number of species. Little is known however about the constraints of this behaviour, e.g. the associated energetic costs. We investigated these costs in long-tailed macaques where alpha males mate guard females to a lesser extent than predicted by the priority of access model. The study was carried out during two mating periods on three wild groups living in the Gunung Leuser National Park, Indonesia. We combined behavioural observations on males' locomotion and feeding activity, GPS records of distance travelled and non-invasive measurements of urinary C-peptide (UCP), a physiological indicator of male energetic status. Mate-guarding led to a decrease in feeding time and fruit consumption suggesting a reduced intake of energy. At the same time, vertical locomotion was reduced, which potentially saved energy. These findings, together with the fact that we did not find an effect of mate-guarding on UCP levels, suggest that energy intake and expenditure was balanced during mate-guarding in our study males. Mate-guarding thus seems to not be energetically costly under all circumstances. Given that in strictly seasonal rhesus macaques, high-ranking males lose physical condition over the mating period, we hypothesise that the energetic costs of mate-guarding vary inter-specifically depending on the degree of seasonality and that males of non-strictly seasonal species might be better adapted to maintain balanced energetic condition year-round. Finally, our results illustrate the importance of combining behavioural assessments of both energy intake and expenditure with physiological measures when investigating energetic costs of behavioural strategies

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