Richard McFarland

Coping with the cold: predictors of survival in wild Barbary macaques, Macaca sylvanus

We report the death of 30 wild Barbary macaques, living in two groups, during an exceptionally cold and snowy winter in the Middle Atlas Mountains, Morocco. We examined whether an individuals time spent feeding, the quality and number of its social relationships, sex and rank predicted whether it survived the winter or not. The time an individual spent feeding and the number of social relationships that an individual had in the group were positive and significant predictors of survival. This is the first study to show that the degree of sociality affects an individuals chance of survival following extreme environmental conditions. Our findings support the view that sociality is directly related to an individuals fitness, and that factors promoting the establishment and maintenance of social relationships are favoured by natural selection.

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.

The Effect of Climatic Factors on the Activity Budgets of Barbary Macaques (Macaca sylvanus)

Climatic conditions can significantly affect the behavior of animals and constrain their activity or geographic distribution. Barbary macaques (Macaca sylvanus) are one of the few primates that live outside the tropics. Here we analyze if and how the activity budgets of Barbary macaques are affected by climatic variables, i.e., air temperature, relative humidity, rainfall, and snow coverage. We collected scan sampling data on the activity budgets of four groups of macaques living in the Middle Atlas Mountains of Morocco from June 2008 to January 2011. This habitat is characterized by extreme seasonal changes, from cold and snowy winters to hot and dry summers. The activity budgets of the macaques differed across months but not across the time of day (with the exception of time spent feeding). The monkeys spent significantly more time feeding or foraging when there was no snow than when snow coverage was moderate or major. Daily rainfall was positively related to resting time and negatively to time spent moving or in social behavior. Air temperature was negatively related to time spent feeding or foraging. Finally, time spent on social behavior was significantly lower when relative humidity was high. These data indicate that environmental factors significantly affect the time budgets of endangered Barbary macaques, a species that has been little studied in the wild. Our findings support previous studies on temperate primates in showing that snow coverage can have negative consequences on the feeding ecology and survival of these species.

Grooming coercion and the post-conflict trading of social services in wild Barbary macaques.

In animal and human societies, social services such as protection from predators are often exchanged between group members. The tactics that individuals display to obtain a service depend on its value and on differences between individuals in their capacity to aggressively obtain it. Here we analysed the exchange of valuable social services (i.e. grooming and relationship repair) in the aftermath of a conflict, in wild Barbary macaques (Macaca sylvanus). The relationship repair function of post-conflict affiliation (i.e. reconciliation) was apparent in the victim but not in the aggressor. Conversely, we found evidence for grooming coercion by the aggressor; when the victim failed to give grooming soon after a conflict they received renewed aggression from the aggressor. We argue that post-conflict affiliation between former opponents can be better described as a trading of social services rather than coercion alone, as both animals obtain some benefits (i.e. grooming for the aggressor and relationship repair for the victim). Our study is the first to test the importance of social coercion in the aftermath of a conflict. Differences in competitive abilities can affect the exchange of services and the occurrence of social coercion in animal societies. This may also help explain the variance between populations and species in their social behaviour and conflict management strategies.

Exploring the Components, Asymmetry and Distribution of Relationship Quality in Wild Barbary Macaques (Macaca sylvanus)

Social relationships between group members are a key feature of many animal societies. The quality of social relationships has been described by three main components: value, compatibility and security, based on the benefits, tenure and stability of social exchanges. We aimed to analyse whether this three component structure could be used to describe the quality of social relationships in wild Barbary macaques (Macaca sylvanus). Moreover, we examined whether relationship quality was affected by the sex, age and rank differences between social partners, and investigated the asymmetric nature of social relationships. We collected over 1,900 hours of focal data on seven behavioural variables measuring relationship quality, and used principal component analysis to investigate how these variables clustered together. We found that relationship quality in wild Barbary macaques can be described by a three component structure that represents the value, compatibility and security of a relationship. Female-female dyads had more valuable relationships and same-age dyads more compatible relationships than any other dyad. Rank difference had no effect on the quality of a social relationship. Finally, we found a high degree of asymmetry in how members of a dyad exchange social behaviour. We argue that the asymmetry of social relationships should be taken into account when exploring the pattern and function of social behaviour in animal societies.

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.

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.

The ‘strength of weak ties’ among female baboons: fitness-related benefits of social bonds

Studies across a range of species have shown that sociability has positive fitness consequences. Among baboons, both increased infant survival and adult longevity have been associated with the maintenance of strong, equitable and durable social bonds. However, not all baboon populations show these patterns of bonding. South African chacma baboons, Papio ursinus, in the Drakensberg Mountains and De Hoop Nature Reserve show cyclical variation in social relations across time, with strong bonds formed only during certain times of the year. Using long-term data from the De Hoop baboons, we tested whether social relations influence female reproductive success in our study group in a manner similar to other baboon populations. Our results show that the number of strong bonds a female maintained predicted birth rate, and that the number of weak bonds a female possessed predicted infant 12-month survival and infant longevity. Fitness-related benefits of sociability were, however, independent of female dominance rank, and there was no relationship between the number of weak and strong bonds a female maintained. One possible explanation for the influence of weak as well as strong bonds in our study group may be that variation in demographic and ecological conditions across populations may favour the use of different social strategies by females. In our sample, weak bonds as well as strong bonds appear to be instrumental to achieving fitness-related benefits.

Assessing the reliability of biologger techniques to measure activity in a free-ranging primate

Assessmentof animal activity patterns can shed lighton a rangeof behavioural and ecological processes. The timing of activity canhelp improve understanding of a species’ spatial ecology, chrono-biology, energetic demands, reproductive strategy and nutritionalrequirements (Halle & Stenseth 2000; Erkert 2003). Activity dataare also useful for the assessment of animal welfare and conser-vation planning (Kitchen & Martin 1996; Broom & Fraser 2007;Cooke 2008); Activity patterns allow us to measure the impact ofhuman disturbance on habitat viability and behaviour (Williamset al. 2006; Yang et al. 2007), and to predict the influence of localor global climate change on the survival and distribution of a spe-cies or population (Walther et al. 2002; Hetem et al. 2012). Reliablemeasures of activity are thus fundamental to furthering our un-derstanding of animal behaviour and ecology.Two main methodological approaches have been used to recordthe activity patterns of free-ranging animals: behavioural obser-vation and biologging (reviewed in Cooke et al. 2004; Nathan et al.2012; Ropert-Coudert et al. 2012). Instantaneous scan sampling(Altmann 1974) is the most commonly used method to record ac-tivity and behaviour data in traditional studies of animal behav-ioural ecology. Scan sampling involves human observers recordingthe activity state (i.e. resting, foraging, travelling or social) of studyanimals at predetermined time intervals, to provide a descriptivemeasure of an individual’s or group’s activity. Scan sampling allowsarangeofbehaviouralinformation(e.g.diet, posture andproximityto conspecifics), in addition to states of activity, to be recordedsimultaneously. However, scan sampling often requires studysubjects to be individually identifiable and habituated to thepresence of human observers, and data can, by definition, only becollected during those periods when human observers are present.These prerequisites for successful scan sampling mayconstrain thecollectionofactivitydata.Insomespeciesorpopulationsitmaynotbe feasible to follow animals regularly, for example, if they arenocturnal or live in an inaccessible habitat, or if the researcher’spresence disrupts normal activity patterns.Biologgers,eitherattachedexternallyorimplantedintheanimal’sbody, have become increasingly popular for recording activityremotely(Cookeetal.2004;Ropert-Coudertetal.2012).Thesedevices

Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.