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Abstract

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 24h amplitude of body temperature) increased, and 24h minima of body temperature decreased, as the 24h minimum ambient temperature decreased. As winter progressed, monkeys became increasingly heterothermic and displayed lower 24h minima of body temperature.Monkeys with a greater number of social partners displayed a smaller 24h amplitude (that is, were more homeothermic) and higher 24h 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.This article is protected by copyright. All rights reserved.

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... Dausmann, 2005;Schmid, 2000;Schmid et al., 2000). More recently, we have used intra-abdominal data loggers to describe the seasonal patterns of core body temperature in wild vervet monkeys (Chlorocebus pygerythrus), the thermoregulatory consequences of both cold and heat stress, interindividual differences in thermal performance, and the importance of behavioral (including social) thermoregulation in body temperature regulation (Henzi et al., 2017;Lubbe et al., 2014;McFarland et al., 2015McFarland et al., , 2019. ...
... The use of intra-abdominal data loggers provides a good index of the thermal status of the body core but requires animals to be captured and to undergo surgical procedures for logger implantation and extraction (see McFarland et al., 2015 for a full description of methods). As an alternative to data logging approaches there has been interest in using infrared thermography to make inferences about thermoregulatory processes in free-ranging animals, including primates (Cilulko et al., 2013;McCafferty, 2007;Narayan et al., 2019;Thompson, Scheidel, et al., 2017). ...
... We removed the data loggers at the end of June 2017. For full details of the capture and surgery procedure see McFarland et al. (2015). Data loggers measured the core intra-abdominal body temperature (to the nearest 5 min) of the same animals that were sampled using the infrared camera. ...
Article
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. Research Highlights • Body surface temperatures do not approximate core body temperatures. • Body surface temperatures tell us more about the local climate a primate is in.
... In recent decades, research has focused on examining the adaptive benefits of differentiated, cooperative and affiliative social ties in animals, beyond the general benefits of social living (Lin & Michener, 1972;Silk, 2007). Studies of several group-living mammals, including primates (Silk et al., 2003(Silk et al., , 2009(Silk et al., , 2010bGilby et al., 2013;McFarland & Majolo, 2013;Archie et al., 2014;McFarland et al., 2015;Lehmann et al., 2016;Kalbitzer et al., 2017;McFarland et al., 2017;Thompson & Cords, 2018), rodents (Weidt et al., 2008;Yee et al., 2008), cetaceans (Foster et al., 2012; and ungulates (Cameron et al., 2009;Vander Wal et al., 2014;Nuñez et al., 2015) have revealed that maintaining affiliative and cooperative ties, both among same and opposite sex partners, corresponds with increased individual fitness, or increased survival and reproductive success. Despite the recent proliferation of findings that 'social ties matter', the mechanisms by which ties influence fitness are not altogether clear. ...
... Simply having more social ties may also increase the number of partners that tolerate bodily contact, enhancing thermoregulation in fluctuating climates. In South Africa, temperatures fall below freezing during winter, and vervets huddle together at night to help maintain homeothermy (McFarland et al., 2015). Vervets that had more spatial and/or grooming partners throughout the day maintained a higher minimum body temperature and varied less in temperature from day to night, as measured by a subcutaneous thermometer. ...
... Nevertheless, the short-term costs of association, like increased aggression received, may be outweighed by a longer-term benefit of a stable affiliative or cooperative tie. One common mechanism that allows ties to passively provide instrumental support is their ability to increase tolerance, allowing individuals to avoid harassment (Duffy et al., 2007;Haunhorst et al., 2017), peaceably co-feed (King et al., 2011;Tiddi et al., 2011;Haunhorst et al., 2017), share safer microhabitats from predators (Kalbitzer et al., 2017) and maintain bodily contact for warmth (McFarland et al., 2015). Ties also provide active instrumental support, such as when females form alliances to defend one another from abusive males (Sterck et al., 1997) or when individuals more effectively communicate the presence of a predator when more strongly bonded with each other . ...
Article
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Many studies highlight the correlation between social ties and fitness, yet often cannot reveal how ties influence fitness. This review is aimed to facilitate the formulation and testing of hypotheses in this area on non-human primates. I outline fitness-relevant measures of social ties and 6 potential pathways from ties to fitness. Pathways include communal care; group level cooperation for resources; monopolizing resources within groups; attaining social status; reducing risk and allostatic load; and developing behavioural competence. Hypotheses for further evaluation include (1) fitness increases sociality, not vice versa; (2) early life experience influences both ties and fitness, (3) ties are actually costly; (4) short term costs of ties are outweighed by long term benefits. With the advance of theoretical and methodological approaches to evaluate the costs and benefits of social ties, and monitor them at multi-generational field sites, primate behavioural ecologists are poised to test several of these hypotheses.
... Physiological processes can be costly in terms of energy expenditure through increased metabolic heat production and water loss through evaporative cooling Levesque et al., 2016). To reduce the physiological costs of thermoregulation, individuals can also engage in behaviors that influence heat exchange with the environment, including changing activity patterns, postural adjustments or selecting thermally-advantageous microclimates (Speakman and Krol, 2010;Huey et al., 2012;McFarland et al. 2015McFarland et al. , 2019aMason et al., 2017Mason et al., , 2020. Behavioral thermoregulation, however, may take place at the expense of other behaviors critical to survival (e.g., feeding, drinking, traveling, and social activity; McFarland et al., 2014;Dunbar et al., 2009). ...
... Given our multiyear dataset on the T b , behavior, and local climate of a wild population, we are uniquely positioned to test NM's ability to predict a wild endotherm's thermal response to the environment. Vervets represent an excellent model to meet this objective, as they experience a wide temperature range in varied environments (Pasternak et al., 2013;McFarland et al., 2014), and possess a range of behavioral and thermoregulatory adaptations (McFarland et al., 2015(McFarland et al., , 2019a(McFarland et al., , 2019b(McFarland et al., , 2020. ...
... Between 2012 and 2016, we collected field data from a population of wild vervet monkeys living on the Samara Private Game Reserve in the Eastern Cape, South Africa (32 • 22 ′ S, 24 • 52 ′ E). We recorded local climate at an onsite weather station (McFarland et al., 2015). This semi-arid region has a seasonal climate, with hot, wet summers, and cold, dry winters. ...
Article
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.
... While these studies provide important insights into the relationship between environmental and behavioral variables, they offer little on the consequences of environmental variability on a primate's physiology, its ability to thermoregulate, or the effectiveness of particular behaviors as buffers against environmental heat or cold. Only a few studies have related thermoregulatory behaviors and activity patterns directly to measures of core body temperature (e.g., Brain & Mitchell, 1999;Dausmann, 2005;Henzi et al., 2017;Lubbe et al., 2014;McFarland et al., 2015;Schmid, 2000;Schmid, Ruf, & Heldmaier, 2000), while others have tended to use skin or subcutaneous temperature measurements to approximate core body temperature (Blanco, Dausmann, Ranaivoarisoa, & Yoder, 2013;Dausmann, Glos, Ganzhorn, & Heldmaier, 2004;Kobbe, Nowack, & Dausmann, 2014;Nowack, Mzilikazi, & Dausmann, 2010;Nowack, Wippich, Mzilikazi, & Dausmann, 2013;Thompson, Williams, Glander, Teaford, & Vinyard, 2014). ...
... To maintain homeothermy in cold environments, autonomic responses include an increase in metabolic heat production, and typically feeding time increases to meet this demand (Campos & Fedigan, 2009;Hill, 2006;Majolo et al., 2013;McFarland et al., 2014). In concert with autonomic responses, primates also employ behavioral thermoregulation, such as huddling that reduces heat loss and sun-basking that increases radiant heat gain (Danzy, Grobler, Freimer, & Turner, 2012;Eppley, Watzek, Dausmann, Ganzhorn, & Donati, 2017;Kelley, Jablonski, Chaplin, Sussman, & Kamilar, 2016;McFarland et al., 2015;Ogawa & Takahashi, 2003;Takahashi, 1997). If energy availability or behavioral mechanisms are insufficient then heat balance is compromised, and changes in the daily pattern of core body temperature become apparent. ...
... Weingrill, Gray, Guo et al., 2018). For example, in our study population of vervet monkeys in the Eastern Cape, South Africa, animals exhibited more variable body temperature rhythms in the winter months than they did in the summer months, despite ambient temperatures regularly exceeding 40 C in summer Lubbe et al., 2014;McFarland et al., 2015). ...
Article
Objectives: Climate change is having a significant impact on biodiversity and increasing attention is therefore being devoted to identifying the behavioral strategies that a species uses to cope with climatic stress. We explore how wild vervet monkeys (Chlorocebus pygerythrus) respond to heat stress, and how behavioral adaptations are used to regulate body temperature. Materials and methods: We implanted wild vervet monkeys with temperature-sensitive data loggers and related the body temperature rhythms of these animals to their use of thermoregulatory behaviors. Results: Environmental temperature had a positive effect on the mean, minima and maxima of daily body temperatures. Environmental temperature had a positive effect on the amount of time that vervet monkeys spent in the shade, and animals that spent more time in the shade had lower body temperature maxima. Drinking water did not have a proximate effect on body temperature, most likely a consequence of their regular access to drinking water. Body temperatures were observed to decrease after swimming events, but tended to return to pre-swim temperatures within 1 hr, suggesting a limited thermal benefit of this behavior. Conclusions: Our data support the view that vervet monkeys cope well in the heat, and use behavior as a means to aid thermoregulation. The ability of primates to be flexible in their use of thermoregulatory behaviors can contribute positively to their capacity to cope with environmental variability. However, given its broad effect on plant productivity and habitat loss, climate change is a major threat to species' biogeographical distribution and survival.
... In a longitudinal study of vervet monkey thermal physiology, 30 adult females (mean body mass = 3.4 kg ± 0.3 s.d.) were implanted with temperature-sensitive biologgers over a 7-year period [28][29][30]. Biologgers instantaneously recorded intra-abdominal T b at five-minute intervals. Normal behaviour resumed on the day after surgery, and no long-term sequelae were observed because of surgeries. ...
... Normal behaviour resumed on the day after surgery, and no long-term sequelae were observed because of surgeries. For details of the capture and surgery procedure, see McFarland et al. [29]. ...
... We entered whether each female gave birth that night as a predictor variable. Body mass was entered as a predictor variable to control for its influence on T b [29]. GLMMs were run using the 'brms' package in R v. 3.5.0. ...
Article
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.
... In the short term, such loss of cohesion can lead to increased aggression 80 . Over time, this disruption could compromise some of the many benefits primates derive from group living, including decreased predation risk, increased foraging efficiency and resource protection, and increased survival rates 75,81,82 . However, the finding that metrics did not uniformly differ across affiliative-and proximity-based networks points to the methodological importance of considering data type and metrics included in network analyses. ...
... Furthermore, males' tendency to be risk-prone will likely facilitate continued frequent proximity to humans. We find that being in proximity to humans and/or provisioning opportunities disrupt macaque social networks, which is especially concerning given affiliative interactions and social bonds in primates are known to provide a suite of fitness benefits, including support from group members during agonistic interactions, increased social ranking, increased reproductive success, increased longevity, increased infant survival, and enhanced thermoregulation during winter 76,77,81 . As such, there are potentially direct fitness implications of such social network disruptions. ...
Article
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Human-wildlife encounters are becoming increasingly frequent across the globe, often leading people to interact with and feed wild animals and impacting animal behaviour and ecology. Although the nature of human-wildlife interactions has been well documented across a number of species, we still have limited understanding as to why some individual animals interact more frequently with humans than others. Additionally, we lack a comprehensive understanding of how these interactions influence animal social networks. Using behavioural data from a group of moor macaque monkeys (Macaca maura), we used permutation-based linear regression analyses to understand how life history and social network factors jointly explain interindividual variation in tendency to interact with humans along a provincial road in South Sulawesi, Indonesia. As our study group spent only a portion of their time in proximity to humans, we also examined how social network structure changes in response to human presence by comparing social networks in the forest to those along the road. We found that sex, individual network position, and associate network position interact in complex ways to influence individual behaviour. Individual variation in tendency to be along the road caused social networks to become less cohesive when in proximity to humans. This study demonstrates that nuanced intragroup analyses are necessary to fully understand and address conservation issues relating to human-wildlife interactions.
... Like other homeothermic endotherms (warm-blooded animals that can regulate their temperature internally), humans also need to keep a relatively constant core body temperature to survive. Studies have shown that nonhuman homeothermic endotherms, like rodents 12 and monkeys 13 , have developed social mechanisms to regulate their core body temperature. A positive correlation between the lower bound of core temperature in colder environments and social network size was found in vervet monkeys, a species often studied because of their similarity to humans 13 . ...
... Studies have shown that nonhuman homeothermic endotherms, like rodents 12 and monkeys 13 , have developed social mechanisms to regulate their core body temperature. A positive correlation between the lower bound of core temperature in colder environments and social network size was found in vervet monkeys, a species often studied because of their similarity to humans 13 . Perhaps unsurprisingly, in humans, there is also a relationship between temperature and social bonds. ...
Article
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In the Human Penguin Project (N = 1755), 15 research groups from 12 countries collected body temperature, demographic variables, social network indices, seven widely-used psychological scales and two newly developed questionnaires (the Social Thermoregulation and Risk Avoidance Questionnaire (STRAQ-1) and the Kama Muta Frequency Scale (KAMF)). They were collected to investigate the relationship between environmental factors (e.g., geographical, climate etc.) and human behaviors, which is a long-standing inquiry in the scientific community. More specifically, the present project was designed to test principles surrounding the idea of social thermoregulation, which posits that social networks help people to regulate their core body temperature. The results showed that all scales in the current project have sufficient to good psychometrical properties. Unlike previous crowdsourced projects, this dataset includes not only the cleaned raw data but also all the validation of questionnaires in 9 different languages, thus providing a valuable resource for psychological scientists who are interested in cross-national, environment-human interaction studies. Machine-accessible metadata file describing the reported data (ISA-Tab format)
... Social preferences towards kin can be driven by the benefits of associating with relatives, such as allomaternal care (reviewed in Briga, Pen, & Wright, 2012;Pope, 2000; and in some cases even brood parasitism, Andersson, 2017), reduced aggression and infanticide risk (Agrell, Wolff, & Ylonen, 1998;reviewed in ;Brown & Brown, 1996), foraging advantages (Griffiths & Armstrong, 2002;Nystrand, 2007), and shared social and ecological knowledge (McComb, Moss, Durant, Baker, & Sayialel, 2001;Salpeteur et al., 2015). However, social associations have also been linked to direct fitness consequences among nonrelatives (Baden, Wright, Louis, & Bradley, 2013;Cameron et al., 2009;Carter & Wilkinson, 2015;McFarland et al., 2015;Riehl, 2011), suggesting that social preferences can evolve based on direct benefits alone. Moreover, evidence for kin-biased relationships in other species, particularly those with higher fissionefusion dynamics, is weak (e.g. ...
Article
Fission–fusion social dynamics are common among a number of vertebrate taxa, and yet the factors shaping these variable associations among subgroup members have not been widely addressed. Associations may occur simply because of shared habitat preferences; however, social ties may also be influenced by genetic relatedness (kinship) or social attraction. Here, we investigate the association patterns of wild black-and-white ruffed lemurs, Varecia variegata, in Ranomafana National Park, Madagascar using behavioural, spatial (home range) and genetic data from 24 individually identified animals. We collected 40 840 records of group composition over a 17-month period and from this calculated pairwise association indices. We also used ranging coordinates and genetic samples to estimate patterns of spatial overlap and kinship, and then related these measures to patterns of affiliation. From these analyses, we found that dyadic ruffed lemur social associations were generally sparse and weak, that home range overlap was minimal and that average relatedness within the community was low. We found no evidence that kinship was related to patterns of either spatial overlap or social association; instead, associations were primarily driven by space use. Moreover, social preferences were unrelated to kinship. While home range overlap explained most of the variation seen in social association, some variation remained unaccounted for, suggesting that other social, ecological and biological factors such as shared resource defence or communal breeding might also play a role in social attraction. Our results further highlight the need to consider individual space use and nuances of species behaviour when investigating social preference and social association more generally.
... Social relationships, described through the content, quality and patterning of social interactions among group members (Hinde 1976) can have a strong impact on individual fitness, especially among group living animals, such as primates (Ostner and Schuelke 2018). Usually, individuals more socially integrated into their group-either via strong or a broad network of social bonds-tend to experience improved physiological wellbeing and health (Smith and Christakis 2008;Brent et al. 2011;McFarland et al. 2015), higher rates of reproductive success (Cameron et al. 2009;McFarland et al. 2017;Page et al. 2017;Ostner and Schuelke 2018) and improved survival Lehmann et al 2016;Ostner and Schuelke 2018). Consequently, the loss of closely connected individuals can have a negative impact on individual health (Christakis and Fowler 2009;Holt-Lunstad et al. 2010), influencing, for example, cardiovascular and pulmonary functions (Uchino 2004). ...
Article
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In recent years, there has been considerable interest in investigating how animal social structure is affected by the loss of individuals. This is often achieved using simulations that generate predictions regarding how the removal of 'key' individuals from a group affects network structure. However, little is known about the effects of such removals in wild and free-ranging populations, particularly the extent to which naturally occurring mortality events and the loss of a large proportion of individuals from a social group affects the overall structure of a social network. Here, we used data from a population of wild Barbary macaques (Macaca sylvanus) that was exposed to an exceptionally harsh winter, culminating in the death of 64% of the adults from two groups. We analysed how social interaction patterns among surviving individuals were affected by the natural loss of group members using social networks based on affiliative (i.e., grooming) and aggressive social interactions. We show that only the structure of the pre-decline grooming networks was conserved in the post-decline networks, suggesting that grooming, but not aggression networks are resilient against the loss of group members. Surviving group members were not significantly different from the non-survivors in terms of their affiliative and agonistic relationships, and did not form assorted communities in the pre-decline networks. Overall, our results suggest that in primates, patterns of affiliative interactions are more resilient to changes in group composition than aggressive interaction patterns, which tend to be used more flexibly in new conditions.
... These can be expressed through seasonal hormonal changes in cortisol and thyroid hormones which affect activity, ranging and foraging patterns, as well as social interactions (e.g. Weingrill et al. 2004;McFarland and Majolo 2013;McFarland et al. 2015;Cristobal-Azkarate et al. 2016; Thompson et al. 2017). ...
Article
Non-human primates (NHPs) can adapt to conditions outside of their natural habitat and climatic ranges but this can be influenced by inherent evolutionary traits or plasticity of species that evolved in diverse environmental conditions. In this study, we investigated how five species of NHPs that have natural distributions across a range of climatic conditions responded to seasonal temperature changes in a captive environment. The activity levels of NHPs were affected by temperature changes over the season, where activity levels were generally reduced at the lower and higher temperature ranges. Species that are naturally found within narrower and warmer climatic ranges, compared to those found in colder environments with wider fluctuations in temperature, showed more marked changes in activity levels in response to temperature changes. In lower temperature conditions, three out of five species showed significantly lower activity levels; whereas in higher temperature conditions, the activity levels of all species did not significantly decrease. The frequency of thermoregulation behaviours was higher, and use of artificial thermoregulatory sources lower, for species that did not substantially adjust their activity levels in different temperature conditions. Our results suggest that NHPs largely retained the evolutionary traits related to thermoregulation, according to the different ambient conditions they evolved in and may have low behavioural plasticity in adapting to conditions outside of their natural ranges. These results provide insights for improving conservation and captive management and may have implications for understanding NHP resilience to the increasing impact of global climate change.
... Table 1. These gregarious primates occupy a semi-arid environment with large seasonal fluctuations of both temperature and rainfall, and similarly show seasonal breeding patterns (Lubbe et al., 2014;McFarland, Barrett, Boner, Freeman, & Henzi, 2014;McFarland et al., 2015). These data were collected by scan samples taken twice every hour for 10 min, during 10-hr days, approximately 3-5 days per week between July 2015 and July 2016. ...
Article
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1. Animal social networks are often used to describe dynamic social systems, where individual behaviour generates network‐level structures that subsequently influence individual‐level behaviour. This interdependence between individual behaviour and group structuring is of central concern for questions concerning the evolution and development of social systems and collective animal behaviour more generally. 2. Various statistical methods exist for estimating network changes through time. One approach, time‐aggregated networks, takes repeated snapshots of interactions within windows of time to generate a time series of networks. However, there remain many analytical hurdles when implementing the time‐aggregated approach. To ameliorate this, we introduce an R package netTS that focuses on three analytical steps for analyzing time‐aggregated networks: choosing appropriate time scale using bootstrapping, comparing patterns to relevant null models using permutation, and finally building and interpreting statistical models using simulated data. We use simulated data to first highlight these steps, then use observed grooming data from a group of vervet monkeys as an applied example. 3.Our results suggest that the use of bootstrapping and permutation can accurately extract known patterns from simulated data. Using this approach with vervet data suggests that there is consistent social structuring, differing from what would be expected due to chance, and that some individuals are contributing to this structure more than others (i.e., keystone individuals). 4. We demonstrate that bootstrapping, permutation, and simulation can aid in constructing and interpreting time‐aggregated networks. We suggest that the use of time‐aggregated networks to quantify patterns of network change can be a useful tool alongside process‐based approaches that seek mechanistic descriptions. Ultimately, by looking at both patterns and processes, dynamic networks can be used to better understand how individual behaviour generates social structures, and in turn how individual behaviour can be influenced by social structures, ultimately leading to a better understanding of the evolution of social behaviour.
... Ties may be particularly important in helping juveniles, in light of their high energetic demands for growth and vulnerability to aggressive competition . In adults, affiliative relationships are often seen to increase tolerance, helping individuals to avoid harassment (e.g., feral horses and Assamese macaques, Cameron et al., 2009;Haunhorst et al., 2017), peaceably co-feed (baboons, King et al., 2011), and maintain body contact for homeothermy (Barbary macaques, Lehmann et al., 2016;McFarland et al., 2015). Close affiliates may also buffer the experience of stressors via socio-positive contact (Crockford et al., 2013;Heinrichs et al., 2003;Hostinar et al., 2014;Kikusui et al., 2006;Young et al., 2014). ...
Article
Primates develop slowly relative to their body size, a pattern posited to result from ecological risk aversion. Little is known, however, about how energy balance contributes to allostatic load in juveniles. Using data collected over 8 consecutive months, we examined variation in energy balance (as measured by urinary C-peptide) and how energy balance, life history status, and social competition related to allostatic load (as measured by deviation from baseline fecal glucocorticoid metabolites, dfGCs) in 41 wild juvenile blue monkeys from 3 social groups. Juvenile energy balance was higher among females, older juveniles, when ripe fruit was more available, and when rainfall was lower. Energy balance, but not life history or competitive environments, predicted dfGC concentrations, such that juveniles generally had lower mean dfGCs when they had higher energy balance. An additional exploratory analysis of how dfGCs relate to social strategies revealed that subjects had lower dfGCs when they groomed less, and played more. Time spent grooming interacted with energy balance in predicting dfGC concentrations, so that individuals that groomed more actually had higher dfGCs when they had higher energy balance. Together these results reveal that energetic deficiencies are a true ecological risk factor in blue monkeys, and suggest that navigating the social environment via overt affiliative behavior is potentially both a stress-relieving and stress-inducing endeavor during development.
... Given previous research, it is also likely that developmental exposures [16] and other behavioural factors beyond sunbathing also mediate the adaptive value of such variants (i.e. diet/feeding, dominance status and social integration [30,89]; sex, body size, residency status, social networks [90]; body position and microhabitat selection [91]; clustering and embracing behaviours [92]). Incorporating genotype data at key loci into already-existing biophysical modelling systems of thermoregulation in wild savannah monkeys [93] could be a relatively simple and effective means of testing these relationships. ...
Article
In the last 300 thousand years, the genus Chlorocebus expanded from equatorial Africa into the southernmost latitudes of the continent, where colder climate was a probable driver of natural selection. We investigated population-level genetic variation in the mitochondrial uncoupling protein 1 ( UCP1 ) gene region—implicated in non-shivering thermogenesis (NST)—in 73 wild savannah monkeys from three taxa representing this southern expansion ( Chlorocebus pygerythrus hilgerti, Chlorocebus cynosuros and Chlorocebus pygerythrus pygerythrus ) ranging from Kenya to South Africa. We found 17 single nucleotide polymorphisms with extended haplotype homozygosity consistent with positive selective sweeps, 10 of which show no significant linkage disequilibrium with each other. Phylogenetic generalized least-squares modelling with ecological covariates suggest that most derived allele frequencies are significantly associated with solar irradiance and winter precipitation, rather than overall low temperatures. This selection and association with irradiance is demonstrated by a relatively isolated population in the southern coastal belt of South Africa. We suggest that sunbathing behaviours common to savannah monkeys, in combination with the strength of solar irradiance, may mediate adaptations to thermal stress via NST among savannah monkeys. The variants we discovered all lie in non-coding regions, some with previously documented regulatory functions, calling for further validation and research.
... Although the majority of body temperature research emphasizes fever and innate immune responses (Palmes and Park 1965;Baracos et al. 1987), body temperature also has critical implications for animal growth (Verbeek 1988;Köhler et al. 2012), reproductive physiology (Royston 1982;Kusuda et al. 2011), body condition (Haftorn 1972, and even social behavior (Gestich et al. 2014). For instance, female vervet monkeys (Chlorocebus pygerythrus) with more social partners exhibited higher minimum body temperatures, which may confer fitness benefits by reducing the costs of homeothermy and increasing energy available for reproduction (McFarland et al. 2015). Critically, body temperature has repercussions for mate competition in both ectotherms and endotherms. ...
Article
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Quantifying the costs of mating is key for understanding life-history trade-offs. As a reflection of metabolic rate, body temperature is one metric for assaying these costs. However, conventional methods for measuring body temperature are invasive and unsuitable for the study of free-living populations of endangered species, including great apes. A promising proxy for body temperature is fecal temperature, the internal temperature of fecal deposits shortly following defecation. We validated this method with humans, finding that maximum fecal temperature is a reliable proxy for rectal temperature. We then applied this method to wild chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. We collected and analyzed 101 fecal temperature measurements from 43 adult chimpanzees (male: N = 28; female: N = 15). Chimpanzee fecal temperature ranged from 33.4 to 38.9 °C, with a mean of 35.8 °C. Although fecal temperature was not predicted by sex, age, or ambient temperature, male fecal temperature was 1.1 °C higher on days when sexually receptive females were present and was positively correlated with male dominance rank. Post hoc analyses showed that overall copulation rates, but not aggression rates, were positively correlated with fecal temperature, suggesting that sexual physiology and behavior best explain mating-related temperature variation. Together, these results indicate fecal temperature is a reliable proxy for core body temperature in large-bodied mammals, captures metabolic costs associated with male mating behavior, and represents a valuable noninvasive tool for biological field research.
... However, even with a methodology adapted to our study group and study site, we could not encompass the full range of group spread forms found at sleeping sites. Additionally, it was difficult to collect data required to test the thermoregulation hypothesis, such as cluster formation, huddling behavior, and body temperature (Campbell et al. 2018;McFarland et al. 2015;Savagian and Fernandez-Duque 2017). Nevertheless, our results raise questions about sleeping tree selection and social thermoregulation by large groups in degraded habitats. ...
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Primates must select sleeping sites carefully to maximize fitness. In habitats with diminished quality and availability of resources, sleeping site selection becomes an even more crucial aspect of primate survival. We investigated sleeping site selection patterns in northern pigtailed macaques (Macaca leonina) living in a degraded habitat by testing the hypotheses of random selection, predation avoidance, and food proximity. We followed a group of northern pigtailed macaques in Sakaerat Biosphere Reserve, northeastern Thailand, over 14 months between February 2017 and October 2018. We identified 107 total sleeping sites and analyzed the forest structure at 50 sleeping sites and 50 randomly selected available sites. While the rate of reuse was low and random (N = 15), with sleeping sites characterized by a low availability of large and tall trees, the selection pattern was not random, with sleeping sites occurring more often in familiar areas (i.e., high site fidelity), and those with a greater number of stems and a higher canopy. These sleeping site characteristics were likely selected to decrease detection by predators and facilitate macaque escape in case of attack, supporting the predator avoidance hypothesis. However, food proximity also played a key role in sleeping site selection in this degraded habitat. Macaques often slept within, or close to, their first/last feeding site and selected their sleeping sites following food distribution, presumably to maximize energy intake. Our results present a new impact of habitat degradation on sleeping site selection in large primate groups: the use of a high number sleeping sites in order to cope with low availability and scattered distribution of fruit resources.
... All individuals are individually recognizable via distinct facial and body markings. Groups are followed for 10 h per day, 5 days per week [20,21]. During the study period for these analyses (April 2015-August 2017), our three groups showed variation in group size: RST = 47-65 (N male = 5-10; N female = 8-15), PT = 33-43 (N male = 3-9; N female = 8-10), RBM = 49-62 (N male = 6-13; N female = 8-18). ...
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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.
... Similar to the social buffering effects described above, prenatal stress effects may be mediated via the benefits of social integration or weak bonds. If prenatally challenged offspring cannot establish relevant network positions it will forgo benefits in terms of enhanced thermoregulation (McFarland et al. 2015), safety from predation , or access to information (McFarland et al. 2017). The lack of these benefits will increase reactive homeostasis (Romero et al. 2009) in the adult offspring which then signals to the next generation. ...
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Prenatal developmental plasticity in response to various environmental and social adversities can affect multiple aspects of offspring phenotype including social behavior strategies with effects that can last into adulthood. Here, we (1) identify adaptive social behavior strategies and their underlying mechanisms as potential targets of developmental plasticity in primates, (2) derive predictions about social behavior outcomes of prenatal adversity from different types of evolutionary models, (3) review the primate evidence for prenatal stress effects on offspring cognitive function, social, and non-social behavior, and (4) discuss avenues for future research. The scarce evidence currently available points towards increased distress behavior, particularly in infant offspring, and reductions of activity, exploration, and affiliative behavior in response to experimental prenatal adversity. Not all effects are stable, the results do not replicate well, and, for the most part, the current data cannot be used to test predictions of evolutionary models because relevant aspects of social behavior were not quantified and not assessed in the complex social environments they evolved for. More comprehensive research in developmental plasticity needs to incorporate sex differences and the interaction of effects from different sensitive periods including adolescence. Moreover, future research needs to assess the role of social buffering in mediating intergenerational effects and trade-offs between the pace of life and social cognitive performance.
... Here we provide new data from a study population close to its latitudinal limits in the semi-arid, temperate Karoo biome of South Africa. This is a region under escalating risk from climate change (Jury, 2013) and is distinctive in its low annual rainfall, very high summer temperatures, and very cold winters (Pasternak et al., 2013;McFarland et al., 2015). Our aim was to describe the primary gastrointestinal parasites recorded from this population and to provide a preliminary assessment of whether prevalence and intensity are linked to sex and social group membership. ...
Article
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).
... Some studies have specifically addressed the effect of ambient temperature on the CRT, mainly because animals Shane K. Maloney et al. that are exposed to extreme heat can exceed their capacity to dissipate heat, while those exposed to extreme cold can exceed their capacity to generate heat. For example, in vervet monkeys, the amplitude of the CRT is positively correlated with the number of days since the start of winter [65]. In that study, it was difficult to separate the effect of exposure to a change in environmental conditions, such as the duration of the exposure to cold ambient temperature, from potential confounders such as a decrease in food availability as winter progressed. ...
Article
In most endothermic homeotherms, core body temperature follows a circadian rhythm. This review focuses on the amplitude of the circadian rhythm of body temperature (CRT) because the amplitude of the CRT has received increasing attention in the last few years. First, we discuss the methodology that can be used to measure the CRT, and the methodology used to calculate the amplitude of the CRT. Then, we illustrate the effect of changes in the external and internal environments on the amplitude of the CRT. Quite interestingly, as illustrated in this paper, while the molecular and hormonal basis of the CRT is well understood, the control of the amplitude is not. We conclude that challenges in the capacity of the animal to thermoregulate, or to manage energy, can impact on the amplitude of the CRT.
... For rodents for example, basic metabolic rate drops considerably when they are experimentally housed with others when in cold environments (Nuñez-Villegas, Bozinovic, & Sabat, 2014). In species other than humans, having a larger social network relates to having higher core temperatures when environmental temperatures drop (McFarland et al., 2015). In humans, there is now also a considerable support for the link between interpersonal relationships and temperature regulation. ...
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Attachment theory was built around the idea that infants rely on others to survive, and it is often forgotten that survival hinged on coping with environmental demands. Adult attachment reports have instead been organized around people’s subjective experience of safety and security in relationships. To resolve the gap between infant’s physical needs and adult attachment experiences, we made a first step by developing the Social Thermoregulation and Risk Avoidance Questionnaire (STRAQ-1) in 12 countries ('N' = 1510), providing a complementary measure to identify biological drives formative to attachment. We conjectured that co-regulatory patterns of temperature and stress are foundational to attachment styles and on this basis used a naïve bootstrapping method to find a robust solution, conducting seven exploratory factor analyses in an exploratory-confirmatory fashion. We identified 23 (out of 57) items in 4 subscales: Social Thermoregulation (Total Omega = .83), High Temperature Sensitivity (.83), Solitary Thermoregulation (.77), and Risk Avoidance (.57). In terms of external validity, we also found that the STRAQ-1 relates to emotion regulation strategies broadly and, importantly, relates to individual differences in attachment specifically, which in turn mediates the relationship with stress and health (making the scale face valid). Our approach provides a robust first effort in identifying biological mechanisms underlying attachment formation.
... They may change social relationships (increasing physical contact with others) within their group to benefit their thermal competences (McFarland et al., 2015), adjust nest architecture to increase thermoregulation (Stewart, Piel, Azkarate, & Pruetz, 2018), preferentially use heat-conserving postures in sunny areas or stay under direct sunlight (Alouatta caraya: Bicca-Marques & Calegaro-Marques, 1998; Callicebus nigrifrons : Gestich, Caselli, & Setz, 2014; P. cynocephalus: Stelzner & Hausfater, 1986), form huddles (Macaca fuscata: Ogawa & Wada, 2011;Ueno & Nakamichi, 2018), select warmer microhabitats during the day (A. palliate: Thompson et al., 2016), or remain for longer in caves (P. ...
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Climatic factors such as temperature and humidity vary seasonally in primate habitats; thus, behavioral adjustments and microhabitat selection by primate species have been interpreted as behavioral adaptations. François' langur (Trachypithecus francoisi), a native species to southwest China and northern Vietnam, inhabits a limestone habitat with extreme climatic conditions. To understand the potential effects of climatic seasonality on this species, we collected data on the individual behavioral budgets in a T. francoisi group between January and December 2010 in Fusui County, China. Monthly, we performed 5–11 days of observation during this period, using focal animal sampling and continuous recording methods. We also recorded ambient temperature (Ta) and relative humidity (Hr) data at our study site. Results indicated that Ta and Hr were significantly correlated with each other and fluctuated dramatically on a daily, monthly, and seasonal basis. The amount of time spent resting, grooming, basking, and huddling also varied on a daily, monthly, and seasonal basis. The proportion of resting time and total sedentary activity time significantly increased at high and low Tas, respectively. The total sedentary time, resting time, and plant branch use all showed positive significant correlations with Ta. Our results suggest that behavioral adjustment and support use of T. francoisi, at least partly, were related to thermoregulation. T. francoisi minimized thermal stress through behavioral adjustments and support use. It is an adaptive behavior associated with the climatic extremes of limestone habitat. This study can potentially advise conservation management strategies in this specific habitat. Conservation efforts should focus on vegetation restoration in langurs' habitat, including those in the foothills.
... Animals often decrease energy expenditure by altering their behavior (e.g. basking, sheltering, huddling, torpor or hibernation) (Dausmann et al. 2004, Hanya et al. 2007, Grueter et al. 2013, Brinkmann et al. 2014, McFarland et al. 2015, Sukhchuluun et al. 2018, or use autonomic response to reduce thermal loss via convection and radiation (e.g. secondary to a reduced skin temperature by triggering cutaneous vasoconstriction) (Schmid andSpeakman 2000, Arnold et al. 2006) or burn stored fat for thermogenesis (Kurita et al. 2002). ...
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Both biotic and abiotic factors play important roles in influencing ecological distributions and niche limits. Where biotic and abiotic stressors co‐occur in space and time, homeostatic systems face a scenario in which stressors can compound to impose a challenge that is greater than the sum of the separate factors. We studied the homeostatic strategies of the golden snub‐nosed monkey Rhinopithecus roxellana, a species living in temperate deciduous forests at the edge of the global distribution range for folivorous primates, to cope with the co‐occurrence of cold temperatures and resource scarcity during winter. We discovered that in winter the monkeys experience a dietary energy deficit of 101 kJ mbm−1 d−1 compared with calculated needs, despite increased feeding. This is partly offset by behavioral changes (reduced locomotion and increased resting) and reducing skin temperature by an average of 3.2°C through a cutaneous vasoconstriction to decrease heat loss. However, their major strategy is ingesting surplus energy and accumulating fat reserves when food was not limiting during summer and autumn. Their 14% of body mass lost over the winter represented an energy yield of 102 kJ mbm−1 d−1, which closely matched the calculated winter energy deficit of 101 kJ mbm−1 d−1. However, the latter value assumes that all the 75.41 kJ mbm−1 d−1 of protein ingested in winter was available for energy metabolism. This is almost certainly an over‐estimate, suggesting that the study population was in negative energy balance over the study period. Our study therefore suggests that despite its suit of integrated homeostatic responses, the confluence of low temperatures and resource limitation during winter places this edge‐of‐range primate close the threshold of what is energetically viable. It also provides a framework for quantitative models predicting the vulnerability of temperate primates to global change.
... Although it might seem reasonable to suggest that a reduction in travel and social time would further help to reduce overall energetic expenditure, the cessation of these activities may not represent a viable option for highly gregarious and mobile species. Traveling with the group provides protection from predators (20) and between-group competitiveness for resources (21) and facilitates other social benefits that might affect individual fitness (22)(23)(24)(25). The increase in traveling time when febrile could also reflect lethargy and the slower pace of a febrile monkey when traveling with the group. ...
Article
Significance Using state-of-the-art biologging technology, we document the occurrence of fevers in wild vervet monkeys and demonstrate that fevers coincide with overt sickness behavior. In so doing, we demonstrate a hidden cost of sociality: Febrile animals were twice as likely to receive aggression from their group mates and were six times more likely to be wounded following the onset of a fever. Sick animals were targeted when least able to fight back, potentially improving the attacker’s social status and further reducing a sick animal’s survival prospects. Understanding disease transmission dynamics requires greater attention to the ways in which social structure can change as a result of infection and how such shifts can influence future patterns of transmission.
... This lack of distinctly individual responses may be because we only sampled adult females who tend to be similarly sized and/or because females, subadults, and juveniles huddle together in their sleep trees (personal obs.), which makes it possible that individuals vary somewhat randomly in their ability to secure a sleep partner across different days (e.g. McFarland et al., 2015). It is also possible that juveniles or adult males might respond differently to this stressor, although previous studies with similarly sized primates have not found substantial differences based on sex alone (Henzi et al., 2017). ...
Article
Environmental challenges are often associated with physiological changes in wildlife that allow animals to maintain homeostasis. Among these, scarcity in resources, and risks from predators, competitors, and humans can all result in psychological and physiological stress. Yet, for habituated species, it is not clear whether this relationship with humans still holds to a lesser degree or is outweighed by the benefits of human presence – such as serving as a buffer from competitors or predators. We investigated how human presence and environmental challenges such as resource availability, weather, predation, and competition may be associated with variation in fecal cortisol metabolite levels (FCMs) in a group of samango monkeys (Cercopithecus albogularis) in the Soutpansberg Mountains, South Africa. FCMs can often broadly track environmental challenges and perturbations. Initially, we employed an exploratory analysis comparing candidate models representing biological hypotheses and found that those incorporating information on human presence had less weight than models for food availability, thermoregulation, and water scarcity. When we examined a subset of the data that included information on intergroup competition and predator alarm calls, we found that FCMs were higher on the day following potential predator encounters but not competitive interactions. As observer numbers increased, responses to predators flattened, indicating that the presence of several humans might deter predators and/or affect samangos' perception of danger – yet we could not distinguish between these possibilities. Together, these results suggest that ecological perturbations track with FCMs in this study population and challenge long-held assumptions that human presence has negligible effects on habituated study animals.
... Lastly, excluding cases of infant death or probable spontaneous abortion, interbirth intervals do not covary with unit size in this population (Tinsley Johnson et al. 2021), suggesting that nutritional variation across group sizes is weak or absent. Instead of suffering intense between-group competition, females in small units could lack sufficient huddling partners (McFarland et al. 2015;Campbell et al. 2018), leading to greater heat loss, increased thermoregulatory expenditures, and delayed maturity. However, if social thermoregulation were poor in small units, we would expect to find increased cold stress in these groups. ...
Article
Female reproductive maturation is a critical life-history milestone, initiating an individual's reproductive career. Studies in social mammals have often focused on how variables related to nutrition influence maturation age in females. However, parallel investigations have identified conspicuous male-mediated effects in which female maturation is sensitive to the presence and relatedness of males. Here, we evaluated whether the more "classic" socioecological variables (i.e., maternal rank, group size) predict maturation age in wild geladas-a primate species with known male-mediated effects on maturation and a grassy diet that is not expected to generate intense female competition. Females delayed maturation in the presence of their fathers and quickly matured when unrelated, dominant males arrived. Controlling for these male effects, however, higher-ranking daughters matured at earlier ages than lower-ranking daughters, suggesting an effect of within-group contest competition. However, contrary to predictions related to within-group scramble competition, females matured earliest in larger groups. We attribute this result to either: 1) a shift to "faster" development in response to the high infant mortality risk posed by larger groups; or 2) accelerated maturation triggered by brief, unobserved male visits. While earlier ages at maturation were indeed associated with earlier ages at first birth, these benefits were occasionally offset by male takeovers, which can delay successful reproduction via spontaneous abortion. In sum, rank-related effects on reproduction can still occur even when socioecological theory would predict otherwise, and males (and the risks they pose) may prompt female maturation even outside of successful takeovers.
... Lastly, excluding cases of infant death or probable spontaneous abortion, interbirth intervals do not covary with unit size in this population (Tinsley Johnson et al. 2021), suggesting that nutritional variation across group sizes is weak or absent. Instead of suffering intense between-group competition, females in small units could lack sufficient huddling partners (McFarland et al. 2015;Campbell et al. 2018), leading to greater heat loss, increased thermoregulatory expenditures, and delayed maturity. However, if social thermoregulation were poor in small units, we would expect to find increased cold stress in these groups. ...
Article
Female reproductive maturation is a critical life-history milestone, initiating an individual's reproductive career. Studies in social mammals have often focused on how variables related to nutrition influence maturation age in females. However, parallel investigations have identified conspicuous male-mediated effects in which female maturation is sensitive to the presence and relatedness of males. Here, we evaluated whether the more "classic" socioecological variables (i.e., maternal rank, group size) predict maturation age in wild geladas-a primate species with known male-mediated effects on maturation and a grassy diet that is not expected to generate intense female competition. Females delayed maturation in the presence of their fathers and quickly matured when unrelated, dominant males arrived. Controlling for these male effects, however, higher-ranking daughters matured at earlier ages than lower-ranking daughters, suggesting an effect of within-group contest competition. However, contrary to predictions related to within-group scramble competition, females matured earliest in larger groups. We attribute this result to either: 1) a shift to "faster" development in response to the high infant mortality risk posed by larger groups; or 2) accelerated maturation triggered by brief, unobserved male visits. While earlier ages at maturation were indeed associated with earlier ages at first birth, these benefits were occasionally offset by male takeovers, which can delay successful reproduction via spontaneous abortion. In sum, rank-related effects on reproduction can still occur even when socioecological theory would predict otherwise, and males (and the risks they pose) may prompt female maturation even outside of successful takeovers.
... A first critical decision facing efforts to study variation in sociality are the types of behavioral data to use when constructing sociality metrics. It is currently debated, exemplified here for studies linking sociality and fitness, whether sociality is best indexed from affinitive behavior alone (Ellis et al. 2017), only from direct affiliative interactions involving body contact like grooming (McFarland et al. 2015), in parallel but separately from both types of data (Bray and Gilby 2020;Brent et al. 2013), from a combination that integrates correlated affinitive and affiliative behaviors (Silk et al. 2006a(Silk et al. , 2010a, or from a combination that also includes agonistic behavior (Crockford et al. 2013). In the following, we will refer to these choices and corresponding behavioral measures as different sociality indices (Box 1). ...
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It has long been recognized that the patterning of social interactions within a group can give rise to a social structure that holds very different places for different individuals. Such within-group variation in sociality correlates with fitness proxies in fish, birds, and mammals. Broader integration of this research has been hampered by the lack of agreement on how to integrate information from a plethora of dyadic interactions into individual-level metrics. As a step towards standardization, we collected comparative data on affinitive and affiliative interactions from multiple groups each of five species of primates to assess whether the same aspects of sociality are measured by different metrics and indices. We calculated 16 different sociality metrics used in previous research and thought to represent three different sociality concepts. We assessed covariation of metrics within groups and then summarized covariation patterns across all 15 study groups, which varied in size from 5 to 41 adults. With some methodological and conceptual caveats, we found that the number of weak ties individuals formed within their groups represented a dimension of sociality that was largely independent from the overall number of ties as well as from the number and strength of the strong ties they formed. Metrics quantifying indirect connectedness exhibited strong covariation with strong tie metrics and thus failed to capture a third aspect of sociality. Future research linking affiliation and affinity to fitness or other individual level outcomes should quantify inter-individual variation in three aspects: the overall number of ties, the number of weak ties, and the number or strength of strong ties individuals form, after taking into account effects of social network density. Significance statement In recent years, long-term studies of individually known animals have revealed strong correlations between individual social bonds and social integration, on the one hand, and reproductive success and survival on the other hand, suggesting strong natural selection on affiliative and affinitive behavior within groups. It proved difficult to generalize from these studies because they all measured sociality in slightly different ways. Analyzing covariation between 16 previously used metrics identified only three rather independent dimensions of variation. Thus, different studies have tapped into the same biological phenomenon. How individuals are weakly connected within their group needs further attention.
... A number of mechanisms have been proposed as possible explanations for positive links between fitness and the differentiated social relationships component of sociability (reviewed by Thompson [24]). These include reduced stress levels, which can improve immune function [25][26][27], protection against predators [28] and against harassment by males [9], thermal benefits [29], and reduced vigilance allowing more time for feeding [13,30]. ...
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In social mammals, social integration is generally assumed to improve females' reproductive success. Most species demonstrating this relationship exhibit complex forms of social bonds and interactions. However, female eastern grey kangaroos ( Macropus giganteus ) exhibit differentiated social relationships, yet do not appear to cooperate directly. It is unclear what the fitness consequences of such sociability could be in species that do not exhibit obvious forms of cooperation. Using 4 years of life history, spatial and social data from a wild population of approximately 200 individually recognizable female eastern grey kangaroos, we tested whether higher levels of sociability are associated with greater reproductive success. Contrary to expectations, we found that the size of a female's social network, her numbers of preferential associations with other females and her group sizes all negatively influenced her reproductive success. These factors influenced the survival of dependent young that had left the pouch rather than those that were still in the pouch. We also show that primiparous females (first-time breeders) were less likely to have surviving young. Our findings suggest that social bonds are not always beneficial for reproductive success in group-living species, and that female kangaroos may experience trade-offs between successfully rearing young and maintaining affiliative relationships.
... Each group was followed for 5 days each week across the study period, and data were collected for 10 h each day (McFarland et al. 2015;Young et al. 2019). To assess changes in activity budget, the behaviour of all visible individuals was recorded during 10-min scan sampling blocks (Altmann 1974) conducted every 30 min throughout the day. ...
Article
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Although sickness behaviour in response to non-lethal parasites has been documented in wild animals, it remains unclear how social and environmental stress might also shape an animal’s behavioural response to parasitism, nor do we know whether simultaneous infection with more than one parasite changes the way animals respond. Here, we combine physiological, environmental, behavioural and parasite measures to investigate behavioural responses to infection in wild vervet monkeys (Chlorocebus pygerythrus) living in a semi-arid region of South Africa. We quantified both activity budget and behavioural predictability to investigate the occurrence of sickness behaviour and infection with two non-lethal gastrointestinal parasite genera. Higher parasite load was linked to an increase in the time spent resting. However, the nature of the relationship with other behaviours was contingent on both the parasite genus in question and parasite species interacted, highlighting the importance of considering co-infection. Overall, food availability was the dominant predictor of behavioural change suggesting that, for monkeys living in a more extreme environment, coping with ecological stress may override the ability to modulate behaviour in response to other physiological stressors. Our findings provide insight into how animals living in harsh environments find ways to cope with parasite infection, avoidance and transmission. Significance statement Sickness behaviour is a suite of behaviours that occur in response to infection that may serve as an adaptive response to cope with infection. For wild animals, the ability to express sickness behaviour will be modulated by the presence of other competing stressors. Hence, the patterns shown are likely to be more complex than under captive conditions, which is where most of our knowledge of sickness behaviour comes from. Using physiological, environmental, behavioural and parasite measures, we demonstrate that although vervet monkeys (Chlorocebus pygerythrus) living in a semi-arid region of South Africa do exhibit sickness behaviours, this is contingent on the parasite genus in question. Further, food availability was the dominant predictor of behavioural change suggesting that, for monkeys living in a more extreme environment, coping with severe ecological stress may override the ability to express sickness behaviour in an adaptive fashion.
... In geladas, we routinely see males and females sit with heads lowered over their chest patches on cold mornings, resulting in less exposed chest patches; they also huddle together with chest patches facing inward, which may also serve to reduce heat loss (Fig. S8). Huddling behavior for thermoregulation has been observed in other primates that live in extreme environments (titi monkeys, Callicebus nigrifrons: Gestich et al. 2014; ring-tailed lemurs, Lemur catta: Kelley et al. 2016); golden snub-nosed monkeys, Rhinopithecus roxellana: Hou et al. 2020) and has been demonstrated to effectively conserve energy expenditure (vervet monkeys, Chlorocebus pygerythrus: McFarland et al. 2015) and increase body temperature (Japanese macaques, Macaca fuscata: Hanya et al. 2007). Although we found that redder chests are associated with higher surface temperatures, we cannot yet determine whether this heat loss incurs a meaningful metabolic cost. ...
Article
Selective pressures have favored conspicuous coloration across a wide variety of taxa. A particularly striking example of conspicuous coloration is the brilliant red chest patch of male geladas (Theropithecus gelada), a species of cercopithecine monkey found in the high-altitude regions of Ethiopia. Previous research found that gelada chest patch redness increases with age (adult vs subadult), social status (“leader” vs non-leader), and mating opportunities (number of adult females), but the mechanism mediating changes in redness has not yet been examined. First, we validated and compared multiple color measurement methods (Adobe Photoshop, micaToolbox designed for use with ImageJ, and a subjective measure using the human eye). Second, we demonstrated that chest patch redness is positively associated with high-intensity physical activity, the application of a heat pack directly to the chest skin, and higher chest skin surface temperatures. Together, these results suggest that increases in chest redness are mediated by increased blood flow to this area with a concomitant increase in surface temperature. Further research is needed to understand both the energetic costs associated with redness and how other males respond to variation in the signal.
... Gregariousness during winter is such a common strategy in a temperate zone, that it must have marked advantages [3,5]. A variety of ultimate and proximate factors have been proposed to explain why gregariousness may evolve during winter. ...
Article
Many animals make behavioural changes to cope with winter conditions, being gregariousness a common strategy. Several factors have been invoked to explain why gregariousness may evolve during winter, with individuals coming together and separating as they trade off the different costs and benefits of living in groups. These trade-offs may, however, change over space and time as a response to varying environmental conditions. Despite its importance, little is known about the factors triggering gregarious behaviour during winter and its change in response to variation in weather conditions is poorly documented. Here, we aimed at quantifying large-scale patterns in wintering associations over 23 years of the white-winged snowfinch Montifringilla nivalis nivalis . We found that individuals gather in larger groups at sites with harsh wintering conditions. Individuals at colder sites reunite later and separate earlier in the season than at warmer sites. However, the magnitude and phenology of wintering associations are ruled by changes in weather conditions. When the temperature increased or the levels of precipitation decreased, group size substantially decreased, and individuals stayed united in groups for a shorter time. These results shed light on factors driving gregariousness and points to shifting winter climate as an important factor influencing this behaviour.
... Gregariousness during winter is such a common strategy in temperate zones that must have marked advantages (Evans and Morand-Ferron, 2019;Mcfarland et al., 2015). A variety of ultimate and proximate factors have been proposed to explain why gregariousness may evolve during winter. ...
... In gregarious species sociality not only offers important positive benefits associated with reducing predation risk [1] and increasing foraging efficiency [2], but also provides additional adaptive benefits by reducing overall metabolic demand [3], providing thermal benefits [4], decreasing stress responses [5] and increasing disease avoidance [6]. It is therefore, generally accepted that an individual's social environment affects a large range of behavioral, psychosocial, and physiological pathways. ...
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This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology ( http://dx.doi.ors/10.24072/pci.evolbiol.100030 ) The influence of oncogenic phenomena on the ecology and evolution of animal species is fast becoming an important research topic. Similar to host-pathogen interactions, cancer negatively affects host fitness, which should lead to the selection of host control mechanisms, including behavioral traits that best minimize the proliferation of malignant cells. Social behavior is one such trait, which is suggested to influence cancer progression. While the ecological benefits of sociality in gregarious species are widely acknowledged, only limited data are available on the role of the social environment on cancer progression. Here, we exposed adult Drosophila , with colorectal-like tumors, to different social environments. First, we show that cancerous flies kept in complete isolation exhibit increased tumor progression. Yet, more surprisingly, we find that cancerous flies, kept in groups with other non-cancerous individuals, also develop tumors at a faster rate compared to those kept with other cancerous conspecifics, suggesting a strong impact of social group composition on cancer growth. Finally, we show that flies can discriminate between individuals at different stages of tumor growth and selectively choose their social environment accordingly. Control flies actively avoid flies with cancer but only at the later stages of tumor development, whereas cancerous flies display strong social interactions with cancerous flies in the early stages of tumor growth. Our study demonstrates the reciprocal links between cancer and social interactions, as well as highlighting how sociality impacts health and fitness in animals and its potential implications for disease ecology and ecosystem dynamics.
... Alternatively, a high local density may act as a cue to habitat quality, such as low predation risk or optimal environmental conditions, causing individuals to prefer patches with higher densities (negative density-dependent dispersal: Stamps 1988Stamps , 1991Muller et al. 1997;Peacor 2003;van Buskirk et al. 2011). In some cases, increased conspecific density may itself be a factor conferring fitness advantages, such as dilution of predation risk or favourable social behaviours (Bygott et al. 1979;Foster & Treherne 1981;Dehn 1990;Hass & Valenzuela 2002;Bilde et al. 2007;McFarland et al. 2015). Kinship can further shape dispersal, strengthening positive density-dependent dispersal to avoid kin competition (Hamilton & May 1977). ...
Article
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Predicting population colonisations requires understanding how spatio‐temporal changes in density affect dispersal. Density can inform on fitness prospects, acting as a cue for either habitat quality, or competition over resources. However, when escaping competition, high local density should only increase emigration if lower‐density patches are available elsewhere. Few empirical studies on dispersal have considered the effects of density at the local and landscape scale simultaneously. To explore this, we analyze 5 years of individual‐based data from an experimental introduction of wild guppies Poecilia reticulata. Natal dispersal showed a decrease in local density dependence as density at the landscape level increased. Landscape density did not affect dispersal among adults, but local density‐dependent dispersal switched from negative (conspecific attraction) to positive (conspecific avoidance), as the colonisation progressed. This study demonstrates that densities at various scales interact to determine dispersal, and suggests that dispersal trade‐offs differ across life stages.
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Changes in abiotic and biotic factors can affect the efficiency of biological systems in animals, forcing them to adjust their behaviors in response to daily and seasonal variations. From September 2016 to August 2017, we collected ranging behavior data on four groups of white-headed langurs (Trachypithecus leucocephalus) in the Guangxi Chongzuo White-Headed Langur National Nature Reserve, Guangxi, southwest China. We simultaneously analyzed how multiple ecological factors affect langur ranging behavior, which should facilitate our understanding of the potential mechanisms underlying their adaptation to limestone habitats. Results showed that langur ranging behavior was significantly affected by diet composition, food availability, and climatic factors. Specifically, moving time and daily path length increased with the increase in dietary diversity. Furthermore, moving time and daily path length were positively associated with the availability of fruit and relative humidity of the forest, and moderately associated with temperature and relative humidity of bare rock. Our study demonstrated that langurs maintain stable moving and feeding times and exhibit a short daily travel distance, likely adopting an energy-conserving behavioral strategy in response to food shortages and high temperatures in the fragmented karst forest. These results highlight the importance of food availability and temperature in shaping the ranging behavior of these karst-dwelling primates.
Article
Parasite and pathogen incidence and prevalence is driven by both periodic variation in environmental conditions and host characteristics. Given the increasing risk of zoonotic transmission to humans, and the close phylogenetic relationship between humans and non‐human primates, understanding this variation in parasite dynamics is becoming essential for epidemiologists and conservationists alike. The extreme seasonal temperatures coupled with declining annual rainfall and severe periodic drought of the semi‐arid Karoo poses distinct challenges to both hosts and pathogens and serves as a window into how animals confront climate change‐induced environmental changes. Here we quantified annual variation in gastrointestinal parasite prevalence, intensity and richness in three troops of wild vervet monkeys (Chlorocebus pygerythrus) and determined what climatic variables were driving these changes. Further, we assessed whether there is long‐term temporal dependence in intra‐individual faecal egg counts. We found variation in the prevalence of five genera of helminths identified in the study population, but little variation in parasite richness across the year. Such variation was driven primarily by precipitation and maximum daily temperature. Finally, we found structure in faecal egg counts, suggesting that contrary to previous findings, egg shedding of Trichostrongylus sp. and ?Protospirura sp. are not stochastic processes and may serve as an indicator of individual levels of infection in our population. Combined, these results provide the first report of seasonal effects in gastrointestinal parasites of vervet monkeys living in an extreme environment. We quantified annual variation in gastrointestinal parasite prevalence, intensity and richness in three troops of wild vervet monkeys (Chlorocebus pygerythrus) living in a semi‐arid environment. We found variation in the prevalence of five genera of helminths identified in the study population, but little variation in parasite richness across the year. This variation was driven primarily by precipitation and maximum daily temperature. We found structure in faecal egg counts which suggests egg shedding of Trichostrongylus sp. and ?Protospirura sp. are not stochastic processes and may serve as an indicator of individual levels of infection in our population. These results provide the first report of seasonal effects in gastrointestinal parasites of vervet monkeys living in an extreme environment.
Chapter
Soziale Ungleichheit und ihre Folgen stellen ein massives Problem für die Stabilität und den Zusammenhalt moderner menschlicher Gesellschaften dar; unter anderem weil sie mit erhöhten Risiken für zahlreiche, individuell nachteilige Merkmale verbunden sind. Wir diskutieren Stress und Einsamkeit als psycho-soziale Faktoren, die diese Verbindung vermitteln, und fassen den Stand der aktuellen Forschung zu deren Beziehungen in Gesellschaften nicht-menschlicher Primaten zusammen. Wir argumentieren, dass die für Homo sapiens vor der Sesshaftigkeit charakteristische Form des Sozialsystems soziale Gleichheit gefördert hat, und dass sich unsere Lebensbedingungen in wenigen Jahrtausenden so rasant und grundlegend geändert haben, dass unsere Psyche und Physiologie noch nicht ausreichend Zeit hatten, darauf mit Anpassungen zu reagieren, die nicht durch die Folgen von chronischem Stress charakterisiert sind. Soziale Ungleichheit und ihre Folgen in menschlichen Gesellschaften liefern also ein Beispiel für die Dynamik der Koevolution zwischen kultureller Veränderung und evolutionärer Anpassung – eines der grundlegenden Probleme der evolutionären Anthropologie.
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Zunächst ist es uns ein Bedürfnis, Gerald Hartung und Matthias Herrgen für die hervorragende Auswahl der Kommentatoren unseres target-Artikels zu danken. Die disziplinäre Vielfalt der fundierten Kommentare war für uns nicht nur überwältigend in Bezug auf die Wahrnehmung der eigenen disziplinären Scheuklappen, sondern auch im Hinblick darauf, dass sie die Faszination und Möglichkeiten einer interdisziplinären Anthropologie verdeutlicht haben. Von daher gilt unser Dank auch den Kommentatoren aus Psychologie, Philosophie, Politikwissenschaften, Ökonomie, Soziologie, Anthropologie und Primatologie für konstruktive Anmerkungen aus dem Blickwinkel ihrer jeweiligen Perspektiven und Expertisen.
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Host social interactions can provide multiple complex pathways for microbial transmission. Here, we suggest non-human primates as models to study the social transmission of commensal or mutualistic microbes due to their high sociality, wide range of group compositions and dominance structures, and diverse group interactions. Microbial sharing from social interactions can positively impact host health by promoting microbial diversity and influencing immunity. Microbes may also drive their own transmission by shaping host behavior, which could lead to fitness benefits for both microbes and hosts. Variation in patterns of social interactions at both the individual and group scale make non-human primates an ideal system to explore the relationship between social behavior, microbial sharing, and their impact on host health and evolution.
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Positive social relationships in humans are known to have health promoting effects while negative social relationships have detrimental effects. Features of the broader social network, including indirect connections, also impact health. However, complicating our ability to examine these features, human networks are diverse and difficult to fully quantify. Animal models where social networks can be fully characterized are useful in examining how structurally similar yet functionally different relationships can differentially relate to biomarkers of health. For example, in nonhuman primates, grooming serves two main functions, to maintain social bonds (family/friends networks) or gain access to resources/support (political networks). We examined whether an individual’s position in these two network types was differentially related to biomarkers of inflammation and physiological stress in female rhesus macaques ( Macaca mulatta ). Consistent with predictions, females with higher family/friends centrality had lower IL-6/TNF-α levels, while females with high political centrality showed elevated levels. Middle-ranking females with high political centrality showed elevated hair cortisol yet little to no benefit of family/friend centrality. These results indicate that while grooming interactions are structurally similar, they may be functionally distinct and therefore have very different, even opposite, effects on health. Affiliative interactions occurring within the context of an established relationship (i.e., family/friends) can provide opportunities for social buffering. In contrast, interactions among individuals without established relationships, even friendly interactions, may ultimately be physiologically costly. Ultimately, these results indicate that while social relationships may appear similar, the underlying functionality can have fundamentally diverse physiological outcomes.
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Environmental challenges in the form of temperature extremes and unusual precipitation, which may lead to prolonged periods outside the thermoneutral zone, can be detrimental to animal physiology. Chacma baboons in the Cape Peninsula of South Africa, one of the highest latitudes at which nonhuman primates are found, experience extremes of both temperature and rainfall, as well as seasonal differences in day length that require animals to condense their daily routine into dramatically reduced daylight hours. Here we examine the effects of these climatic factors on the behavior (activity budgets and foraging patterns) and physiology (fecal glucocorticoid concentrations) of adult females (N = 33) in three groups of chacma baboons (Papio ursinus) inhabiting the Cape Peninsula, where temperatures ranged from 7 to 39 °C, monthly rainfall ranged from 2 to 158 mm, and day length varied by 4.5 h across seasons. Climatic variables showed a clear relationship to female baboon glucocorticoid concentrations, which significantly increased with lower temperatures, higher rainfall and shorter day lengths. Activity budgets also differed between summer and winter, with females generally spending less time socializing, moving and resting in the winter compared to summer, with some differences between troops in their feeding-related activities. Cold temperatures accompanied by rainfall and short day lengths may thus represent an ecological constraint for this population. This study highlights the potential impact of anthropogenic climate change on the physiology, behavior, and, ultimately, survival of wildlife populations.
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Animals show various forms of behavioral thermoregulation to minimize cold stress. Given that higher dominance rank is often associated with increased fitness in group-living animals, higher-ranking individuals may also benefit from better access to thermally optimal spatial positions within huddles. This study examined the association between dominance rank and the potential thermoregulatory benefits of huddling behavior in Japanese macaques (Macaca fuscata) inhabiting Shodoshima Island, which form exceptionally large huddles. I photographed monkey huddles, and analyzed the number of individuals that males were in contact with and males’ spatial positons in huddles. Higher-ranking males were significantly more likely to be in contact with larger numbers of individuals in huddles. Higher-ranking males occupied non-peripheral positions in huddles more often than lower-ranking males, which put them in contact with larger numbers of individuals. These results suggest that high dominance rank may confer potential thermal advantages on male Japanese macaques. The mechanism for this is likely that the highest-ranking male often intrude in already-formed huddles, although such behaviors of males were not quantitatively assessed. This study contributes to a better understanding of the mechanisms of cold adaptation in relation to dominance rank in group-living animals.
Article
Males in female-philopatric social groupings leave their natal groups to pursue successive reproductive opportunities in one or more other groups. In vervet monkeys, Chlorocebus pygerythrus, adult males coexist and physical eviction is not a driver of male movement. Migratory decisions are expected to turn on an evaluation of future reproductive opportunity, as indexed principally by local operational sex ratio and relative competitive ability. Although vervet males' reproductive success is correlated with dominance, they are distinctive in that the attainment of rank is contingent on integration into female sociospatial networks and we expect decisions about continued residency to reflect this. We used 8 years' data from three groups to confirm that male dispersal between groups is seasonal in our population, with a peak that is coterminous with androgen levels and precedes peak mating and conception by 4 weeks. The average length of completed residency was 459 days, with an increase in the logged rate of departure after 1428 days, which is 150 days longer than the estimated modal age at first conception by putative daughters. There were positive correlations between a male's initial and highest rank, and between his highest rank and the length of time to reach it. We found that a male's residency was positively and independently associated with his highest achieved rank and both his grooming centrality and proximity degree. Additionally, increasing rank and proximity degree also had positive effects on residency length subsequent to the attainment of his highest rank. The probability of emigration was associated negatively with both female number and grooming centrality scores. We conclude that emigration from a group is linked to male rank attainment and mediated by a male's integration into female sociospatial networks. We found no evidence that emigration preceded the sexual maturity of putative daughters.
Article
Many species use social interactions to cope with challenges in their environment and a growing number of studies show that individuals which are well-connected to their group have higher fitness than socially isolated individuals. However, there are many ways to be 'well-connected' and it is unclear which aspects of sociality drive fitness benefits. Being well-connected can be conceptualized in four main ways: individuals can be socially integrated by engaging in a high rate of social behaviour or having many partners; they can have strong and stable connections to favoured partners; they can indirectly connect to the broader group structure; or directly engage in a high rate of beneficial behaviours, such as grooming. In this study, we use survival models and long-term data in adult female rhesus macaques (Macaca mulatta) to compare the fitness outcomes of multiple measures of social connectedness. Females that maintained strong connections to favoured partners had the highest relative survival probability, as did females well-integrated owing to forming many weak connections. We found no survival benefits to being structurally well-connected or engaging in high rates of grooming. Being well-connected to favoured partners could provide fitness benefits by, for example, increasing the efficacy of coordinated or mutualistic behaviours.
Article
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.
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Pair bonding (i.e. individuals showing a preference for a specific opposite-sex individual) has been demonstrated in several socially monogamous species. However, social bonds also occur in nonmonogamous species, but have received less attention. Currently, we do not know whether social bonds in monogamous pairs differ from social bonds in polygynous groups. We studied the socially flexible African striped mouse in the laboratory, conducting 3 h partner preference tests typically used to measure pair bonds in socially monogamous prairie voles, Microtus ochrogaster. In the field, striped mice typically live in polygynous groups, but socially monogamous pairs have also been observed. We compared social bonds between 12 monogamous pairs and 12 polygynous groups (1 male and 2 females). The social situation (monogamous versus polygynous) did not influence social bonds. Female striped mice showed a preference for their partner. While males spent more time in body contact with their partner, they showed a sexual preference for strange females. Polygynous males did not show a preference for one of their two females. While significant preferences for partners were found in striped mice, social preference was less strong than that reported for socially monogamous prairie voles. In summary, our results suggest that opposite-sex social bonds not only occur in monogamous species but also in species that live in polygynous groups, but that these bonds might be weaker in polygynous species.
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Social animals need connection Much research over the past decade or so has revealed that health and lifespan in humans, highly social animals, are reduced with social adversity. We humans are not the only animals that are social, however, and similar research has shown that other social mammals are similarly influenced by isolation and adversity. Snyder-Mackler et al. reviewed the relationships between social environment and many aspects of health and well-being across nonhuman mammals and investigated the similarities between these and patterns in humans. They found many of the same threats and responses across social mammals. Science , this issue p. eaax9553
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Cambridge Core - Animal Behaviour - Savanna Monkeys - by Trudy R. Turner
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Networks are often used to describe adaptive social systems, where individual (node) behaviour generates network-level structures that influence subsequent individual-level behaviour. To address questions about the dynamics of network structure in these systems, there is a need to analyze networks through time. Various statistical methods exist for estimating the behaviour of networks in time, in terms of both time-ordered and time-aggregated networks. In this paper, we discuss three main analytical steps for the analysis of time-aggregated network data: 1) aggregation choices, 2) null-model comparisons, and 3) constructing, parameterizing, and making inferences from time series models. We then present a custom R package, netTS, which facilitates these steps. Observed grooming data from a group of vervet monkeys, a highly social primate species, is used as an example to highlight three potential analyses: 1) quantifying the stability of network-level social structures through time, 2) identifying keystone nodes driving/maintaining network structures, and 3) quantifying the interdependence between node behaviour through time. In particular, we highlight the role of bootstrapping, permutation, and simulation as critical components in the analysis of time-aggregated networks.
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Flamingos are well known for their gregarious habits and aggregations in large flocks, but evaluation of the mechanisms behind social grouping remain poorly understood. Captive birds provide a useful model for investigating aspects of social choice in highly gregarious, long-lived species. Animals invest in social relationships that convey fitness benefits and bonds can be long-lasting. For some species, field-based measurement of social networks can be difficult. Captive populations therefore provide a useful alternative for measuring social choices. Data were collected on flamingos at WWT Slimbridge Wetland Centre from 2013 to 2016 and compared to data from 2012. For three flocks, associations were analysed along with individual foot health scores to identify any relationship between health and social behaviour. Long-term partnerships were present in all flocks; preferred associates noted in 2012 were present in 2016. Matrix correlations across years were positive; arrangements of dyads, trios and quartets with higher ties strengths were visible at the beginning and end of the study. Both male-male and female-female bonds were stable over time. All flamingos were more frequently seen socialising than solitary; those in the largest flock showed the highest occurrence of social behaviour (irrespective of enclosure size differences). The number of connections realised from all available within a network was significantly influenced by season. Foot health did not predict associations in these three flamingo networks. Our results indicate that flamingo societies are complex (i.e. formed of long-standing preferential partnerships and not loose, random connections) and the impact of flock size and environment on sociality should be investigated further. These results are helpful for those working with captive flamingos to consider the number of birds housed so that an array of opportunities for choice of associate and/or breeding partner are available in zoo-housed flocks.
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Narrow riparian woodlands along non-perennial streams have made it possible for vervet monkeys to penetrate the semi-arid karoo ecosystem of South Africa, whilst artificial water points have more recently allowed these populations to colonize much more marginal habitat away from natural water sources. In order to better understand the sequelae of life in these narrow, linear woodlands for historically 'natural' populations and to test the prediction that they are ecologically stressed, we determined the size of troops in relation to their reliance on natural and artificial water sources and collected detailed data from two river-centred troops on activity, diet and ranging behaviour over an annual cycle. In comparison to other populations, our data indicate that river-centred troops in the karoo were distinctive primarily both for their large group sizes and, consequently, their large adult cohorts, and in the extent of home range overlap in what is regarded as a territorial species. Whilst large group size carried the corollary of increased day journey length and longer estimated interbirth intervals, there was little other indication of the effects of ecological stress on factors such as body weight and foraging effort. We argue that this was a consequence of the high density of Acacia karroo, which accounted for a third of annual foraging effort in what was a relatively depauperate floristic habitat. We ascribed the large group size and home range overlap to constraints on group fission. Conservation implications: The distribution of group sizes, sampled appropriately across habitats within a conservation area, will be of more relevance to management than average values, which may be nothing more than a statistical artefact, especially when troop sizes are bimodally distributed.
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OBJECTIVE:The objective of the study was to assess the roles of social stress and social status in susceptibility to upper respiratory infection. METHOD: Sixty male cynomolgus monkeys were randomly assigned to stable or unstable social conditions for 15 months. Two markers of social status, social rank and percent of behaviors that were submissive, were assessed at independent observation periods. Endocrine, immune, and behavioral responses were each assessed (at 3-month intervals) during the 9th through 14th months of the study. At the beginning of the 15th month, all animals were exposed to a virus (adenovirus) that causes a common-cold-like illness. The primary outcome was whether or not an animal developed an infection (shed virus) after viral exposure. RESULTS:Although the social instability manipulation was associated with increased agonistic behavior as indicated by minor injuries and elevated norepinephrine responses to social reorganizations, the manipulation did not influence the probability of being infected by the virus. However, low social status (as assessed by either marker) was associated with a substantially greater probability of being infected. It was also associated with less body weight, greater elevated cortisol responses to social reorganizations, and less aggressive behavior. However, none of these characteristics could account for the relation between social status and infection. CONCLUSIONS: Social stress was not associated with susceptibility to infection. However, animals with lower social status were at higher risk than high social status animals.
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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 individual's 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 individual's chance of survival following extreme environmental conditions. Our findings support the view that sociality is directly related to an individual's fitness, and that factors promoting the establishment and maintenance of social relationships are favoured by natural selection.
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Primate social life and behaviour is contingent on a number of levels: phylogenetic, functional and proximate. Although this contingency is recognized by socioecological theory, variability in behaviour is still commonly viewed as 'noise' around a central tendency, rather than as a source of information. An alternative view is that selection has acted on social reaction norms that encompass demographic variation both between and within populations and demes. Here, using data from vervet monkeys (Chlorocebus aethiops pygerythrus), we illustrate how this alternative approach can provide a more nuanced account of social structure and its relation to contingent events at the ecological and demographic levels. Female vervets in our South African study population live in large groups, where they experience demographic stress and increased levels of feeding competition relative to an East African population in Amboseli, Kenya. Females in the South African population did not respond to this stress by intensifying competition for high-value grooming partners to help alleviate the effects of this stress, did not show the expected rank-related patterns of grooming, nor did they show any spatial association with their preferred grooming partners. Increased group size therefore resulted in a reorganization of female social engagement that was both qualitatively and quantitatively different to that seen elsewhere, and suggests that female vervets possess the flexibility to shift to alternative patterns of social engagement in response to contingent ecological and demographic conditions.
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We developed interpolated climate surfaces for global land areas (excluding Antarctica) at a spatial resolution of 30 arc s (often referred to as 1-km spatial resolution). The climate elements considered were monthly precipitation and mean, minimum, and maximum temperature. Input data were gathered from a variety of sources and, where possible, were restricted to records from the 1950-2000 period. We used the thin-plate smoothing spline algorithm implemented in the ANUSPLIN package for interpolation, using latitude, longitude, and elevation as independent variables. We quantified uncertainty arising from the input data and the interpolation by mapping weather station density, elevation bias in the weather stations, and elevation variation within grid cells and through data partitioning and cross validation. Elevation bias tended to be negative (stations lower than expected) at high latitudes but positive in the tropics. Uncertainty is highest in mountainous and in poorly sampled areas. Data partitioning showed high uncertainty of the surfaces on isolated islands, e.g. in the Pacific. Aggregating the elevation and climate data to 10 arc min resolution showed an enormous variation within grid cells, illustrating the value of high-resolution surfaces. A comparison with an existing data set at 10 arc min resolution showed overall agreement, but with significant variation in some regions. A comparison with two high-resolution data sets for the United States also identified areas with large local differences, particularly in mountainous areas. Compared to previous global climatologies, ours has the following advantages: the data are at a higher spatial resolution (400 times greater or more); more weather station records were used; improved elevation data were used; and more information about spatial patterns of uncertainty in the data is available. Owing to the overall low density of available climate stations, our surfaces do not capture of all variation that may occur at a resolution of 1 km, particularly of precipitation in mountainous areas. In future work, such variation might be captured through knowledge-based methods and inclusion of additional co-variates, particularly layers obtained through remote sensing.
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In addition to sexual selection, selection resulting from social interactions in contexts other than mating can be a potent evolutionary force. Such social selection processes are facilitated whenever individual fitness varies as a result of any form of social interactions. The choice of social partners for communal care of young is such a situation in which interactants potentially experience fitness variance. In this study, we investigated the existence and impact of female social partner choice and the potential for social selection to occur in the cooperatively breeding wild house mouse, Mus domesticus. We analysed patterns of individual associations in groups of females, and compared the reproductive behaviour of females grouped with either a preferred or a nonpreferred social partner over an experimental life span of half a year, using spatial association as a measure of preference. We predicted low reproductive competition among preferred social partners and high competition, reflected in lower reproductive success, among nonpreferred. Our results showed that female house mice displayed nonrandom preferences, and that social partner choice yielded significant fitness benefits. Females in pairs with a preferred partner had a significantly higher probability to give birth and to establish an egalitarian, cooperative relationship, resulting in higher reproductive success than females in nonpreferred pairs. This suggests that interactions among females are subject to social selection processes, driving the evolution of female traits.
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The evolutionary forces that drive fitness variation in species are of considerable interest. Despite this, the relative importance and interactions of genetic and social factors involved in the evolution of fitness traits in wild mammalian populations are largely unknown. To date, a few studies have demonstrated that fitness might be influenced by either social factors or genes in natural populations, but none have explored howthe combined effect of social and genetic parameters might interact to influence fitness. Drawing from a long-term study of wild bottlenose dolphins in the eastern gulf of Shark Bay,Western Australia, we present a unique approach to understanding these interactions. Our study shows that female calving success depends on both genetic inheritance and social bonds. Moreover, we demonstrate that interactions between social and genetic factors also influence female fitness. Therefore, our study represents a major methodological advance, and provides critical insights into the interplay of genetic and social parameters of fitness.
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In many mammals, females form close social bonds with members of their group, usually between kin. Studies of social bonds and their fitness benefits have not been investigated outside primates, and are confounded by the relatedness between individuals in primate groups. Bonds may arise from kin selection and inclusive fitness rather than through direct benefits of association. However, female equids live in long-term social groups with unrelated members. We present 4 years of behavioral data, which demonstrate that social integration between unrelated females increases both foal birth rates and survival, independent of maternal habitat quality, social group type, dominance status, and age. Also, we show that such social integration reduces harassment by males. Consequently, social integration has strong direct fitness consequences between nonrelatives, suggesting that social bonds can evolve based on these direct benefits alone. Our results support recent studies highlighting the importance of direct benefits in maintaining cooperative behavior, while controlling for the confounding influence of kinship.
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Sociality has evolved in many animal taxa, but primates are unusual because they establish highly differentiated bonds with other group members. Such bonds are particularly pronounced among females in species like baboons, with female philopatry and male dispersal. These relationships seem to confer a number of short-term benefits on females, and sociality enhances infant survival in some populations. However, the long-term consequences of social bonds among adult females have not been well established. Here we provide the first direct evidence that social relationships among female baboons convey fitness benefits. In a group of free-ranging baboons, Papio cynocephalus ursinus, the offspring of females who formed strong social bonds with other females lived significantly longer than the offspring of females who formed weaker social bonds. These survival benefits were independent of maternal dominance rank and number of kin and extended into offspring adulthood. In particular, females who formed stronger bonds with their mothers and adult daughters experienced higher offspring survival rates than females who formed weaker bonds. For females lacking mothers or adult daughters, offspring survival was closely linked to bonds between maternal sisters. These results parallel those from human studies, which show that greater social integration is generally associated with reduced mortality and better physical and mental health, particularly for women.
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The yellow-bellied marmot (Marmota flaviventris) is a social, ground-dwelling squirrel that lives either individually or in kin groups of from two to five adult females. Philopatry and daughter recruitment lead to the formation and persistence of matrilines at habitat sites. By using 37 years of demographic data for 12 habitat sites, we could determine long-term trends in the effects of group size on two measures of fitness, survivorship and net reproductive rate, which otherwise are obscured by annual fluctuations in these measures. Both size and number of matrilines varied among sites and survivorship and net reproductive rate varied among sites and among matriline sizes. The role of social organization was explored further by examining the effect of matriline size, averaged over all years and sites, on fitness. For both survivorship and net reproductive rate the relationship with matriline size was curvilinear. Fitness increased with the increase in matriline size and then decreased in the largest groups. Decreased fitness in matrilines of four or five was associated with agonistic behavior, a large number of 2-year-old females in the social group, and reproductive suppression. There is no evidence that females acted to increase their fitness by increasing indirect fitness; i.e., by assisting relatives, but attempted to increase direct fitness. Direct fitness increased when mortality and fission of large matrilines reduced group size and the surviving females increased reproduction.
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Endotherms maintain constant body temperature through physiological and behavioral adjustments. Behavioral thermoregulation is an important factor influencing energy balance. We exposed the leaf-eared mouse, Phyllotis darwini, to temperatures corresponding to its natural thermal range and studied two forms of behavioral thermoregulation: diminishing surface to volume ratio by huddling and heat dissipation by increasing physical contact with the substrate (flattening). We predicted that at low ambient temperatures (T(a)) huddling would be used as a heat conservation mechanism and at high T(a) flattening would be used for heat loss. We simultaneously measured oxygen consumption (VO2) and flattening, in response to three independent factors: huddling, T(a), and body mass. Each experiment was a 6-h VO2 trial where five virgin females were measured at constant T(a). We performed this protocol for two body mass groups, small (ca. 40 g) and large (ca. 70 g), in a metabolic chamber. Treatments were groups with and without the ability to huddle at five different T(a), ranging from 5 degrees to 35 degrees C. A significant interaction between all three factors was found. Huddling and flattening were used as strategies for conserving or dissipating heat, respectively, and the shift between both strategies occurred at the lower limit of thermoneutrality. At T(a) below thermoneutrality, huddling was a more effective way of reducing metabolic requirements and was more efficient (H(E)) in small individuals than large individuals. So, by huddling, small individuals save more energy. At high T(a), flattening appeared to be an equally useful mechanism for heat loss, for both large and small animals.
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Among nonhuman primates, females often form strong bonds with kin and other group members. These relationships are thought to have adaptive value for females, but direct effects of sociality on fitness have never been demonstrated. We present 16 years of behavioral data from a well-studied population of wild baboons, which demonstrate that sociality of adult females is positively associated with infant survival, an important component of variation in female lifetime fitness. The effects of sociality on infant survival are independent of the effects of dominance rank, group membership, and environmental conditions. Our results are consistent with the evidence that social support has beneficial effects on human health and well-being across the life span. For humans and other primates, sociality has adaptive value.
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Social stress is associated with development of many psychological and physiological disturbances in humans. Animal models are needed to determine the etiology of these diseases and to develop rational clinical therapies to treat those afflicted. Rodent and non-human primate models of social stress have been developed to address these needs and contribute in complementary ways to the understanding of social stress. In this review, we provide an overview of common rodent and non-human primate models of social stress used in the laboratory with a focus on social hierarchy models. The implications of the current findings on understanding of the development of stress-related disease will also be discussed.
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Mammals generally profit from social thermoregulation, and the primary benefit of sociality during hibernation is thought to be the reduction of metabolic demands during periodic arousals. It has even been postulated that the energetic advantages during hibernation might have been the driver for the evolution of sociality in some mammal species.As the necessity to show arousals and the concurring energetic costs depend on the temperature regime in the hibernacula, we tested whether this is also a plausible scenario in tropical hibernators such as the Malagasy lemur Cheirogaleus medius, with comparatively high and often fluctuating temperature regimes in their hibernacula.To this end, we studied group composition and energy budgets (skin temperature patterns, metabolic rate) over three hibernation and activity seasons in a total of 53 free-ranging C. medius.Our results show that C. medius mostly occupied tree hollows solitarily during hibernation, contrary to the active season, and that the energetic savings were comparable for individuals hibernating socially in groups or solitarily (both about 74% compared to the resting metabolic rate of the active season). However, in larger groups hibernation patterns were less regular and synchronized and individual torpor-arousal cycles were more frequently interrupted by euthermic group members than in individuals hibernating solitarily or in pairs.We conclude that sociality during hibernation is not necessarily driven by energetic demands, and might even be energetically disadvantageous in tropical species (at least in larger groups). Other factors, like social coherence or ecological and behavioural constraints, may be of greater influence for the evolution of sociality under tropical conditions.This article is protected by copyright. All rights reserved.
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We used implanted miniature data loggers to obtain the first measurements of body temperature from a free-ranging anthropoid primate. Vervet monkeys (Chlorocebus pygerythrus) living in a highly seasonal, semi-arid environment maintained a lower mean 24-h body temperature in winter (34.6 ± 0.5 °C) than in summer (36.2 ± 0.1 °C), and demonstrated increased heterothermy (as indexed by the 24-h amplitude of their body temperature rhythm) in response to proximal environmental stressors. The mean 24-h amplitude of the body temperature rhythm in summer (2.5 ± 0.1 °C) was lower than that in winter (3.2 ± 0.4 °C), with the highest amplitude for an individual monkey (5.6 °C) recorded in winter. The higher amplitude of the body temperature rhythm in winter was a consequence primarily of lower 24-h minimum body temperatures during the nocturnal phase, when monkeys were inactive. These low minimum body temperatures were associated with low black globe temperature (GLMM, β = 0.046, P < 0.001), short photoperiod (β = 0.010, P < 0.001) and low rainfall over the previous 2 months, which we used as a proxy for food availability (β = 0.001, P < 0.001). Despite the lower average winter minimum body temperatures, there was no change in the lower modal body temperature between winter and summer. Therefore, unlike the regulated physiological adjustments proposed for torpor or hibernation, these minimum winter body temperatures did not appear to reflect a regulated reduction in body temperature. The thermoregulatory plasticity nevertheless may have fitness benefits for vervet monkeys.
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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. Am J Phys Anthropol, 2014. © 2014 Wiley Periodicals, Inc.
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Mammals exposed to low temperatures increase their metabolic rate to maintain constant body temperature and thus compensate heat loss. This high and costly energetic demand can be mitigated through thermoregulatory behavior such as social grouping or huddling, which helps to decrease metabolic rate as function of the numbers of individuals grouped. Sustained low temperatures in endothermic animals produce changes over time in rates of energy expenditure, by means of phenotypic plasticity. However, the putative modulating effect that huddling exerts on the flexibility of the basal metabolic rate (BMR) due to thermal acclimation remains unknown. We determined BMR values in Octodon degus, an endemic Chilean rodent, after being acclimated either to 15°C or 30°C during 60 days, both alone and in groups of 3 and 5 individuals. At 15°C, BMR of huddling individuals was 40% lower than that of animals housed alone. Moreover, infrared thermography revealed a significant increase in local surface temperatures in huddled animals. Furthermore, individual thermal conductance was lower in individuals acclimated to 15°C than at 30°C, but no differences were observed between single and grouped animals. Our results indicate that huddling prevent an increase in BMR when animals are acclimated to cold conditions and that this effect is proportional to the number of animals grouped.
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We report the first experimental study of the effect of long-term (over 2 years) exposure to a stressor on cellular immune response. Forty-three male cynomolgus monkeys were randomly assigned to stable or unstable social conditions for 26 months. The proportion of time spent in affiliative behaviors was assessed by observations made twice weekly. T-cell immune response (mitogen-stimulated cell proliferation) was assessed weekly for 3 weeks immediately following the 26-month manipulation. The possibility that affiliative behavior represents an attempt to cope with social stress was supported by greater affiliation among animals in the unstable condition than in the stable condition. Animals in the unstable condition also demonstrated relatively suppressed immune response. More affiliative animals showed enhanced immune response, with the beneficial effects of affiliation occurring primarily among unstable animals. The data are interpreted as consistent with the stress-buffering hypothesis; that is, affiliation protects animals from the potentially pathogenic influences of chronic social stress.
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Seven major types of sampling for observational studies of social behavior have been found in the literature. These methods differ considerably in their suitability for providing unbiased data of various kinds. Below is a summary of the major recommended uses of each technique: In this paper, I have tried to point out the major strengths and weaknesses of each sampling method. Some methods are intrinsically biased with respect to many variables, others to fewer. In choosing a sampling method the main question is whether the procedure results in a biased sample of the variables under study. A method can produce a biased sample directly, as a result of intrinsic bias with respect to a study variable, or secondarily due to some degree of dependence (correlation) between the study variable and a directly-biased variable. In order to choose a sampling technique, the observer needs to consider carefully the characteristics of behavior and social interactions that are relevant to the study population and the research questions at hand. In most studies one will not have adequate empirical knowledge of the dependencies between relevant variables. Under the circumstances, the observer should avoid intrinsic biases to whatever extent possible, in particular those that direcly affect the variables under study. Finally, it will often be possible to use more than one sampling method in a study. Such samples can be taken successively or, under favorable conditions, even concurrently. For example, we have found it possible to take Instantaneous Samples of the identities and distances of nearest neighbors of a focal individual at five or ten minute intervals during Focal-Animal (behavior) Samples on that individual. Often during Focal-Animal Sampling one can also record All Occurrences of Some Behaviors, for the whole social group, for categories of conspicuous behavior, such as predation, intergroup contact, drinking, and so on. The extent to which concurrent multiple sampling is feasible will depend very much on the behavior categories and rate of occurrence, the observational conditions, etc. Where feasible, such multiple sampling can greatly aid in the efficient use of research time.
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Highlights ► Assessment of monthly and hourly activity patterns in wild vervet monkeys. ► Scan sampling and biologging provide comparable measures of monthly activity. ► Scan sampling and biologging provide comparable measures of hourly activity. ► Validation of biologger methods in their measurement of activity.
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People are interconnected, and so their health is interconnected. In recognition of this social fact, there has been growing conceptual and empirical attention over the past decade to the impact of social networks on health. This article reviews prominent findings from this literature. After drawing a distinction between social network studies and social support studies, we explore current research on dyadic and supradyadic network influences on health, highlighting findings from both egocen-tric and sociocentric analyses. We then discuss the policy implications of this body of work, as well as future research directions. We conclude that the existence of social networks means that people's health is inter-dependent and that health and health care can transcend the individual in ways that patients, doctors, policy makers, and researchers should care about.
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We studied huddling of Tibetan macaques (Macaca thibetana) at a sleeping site in Huangshan, China, during the mating and birth seasons. Tibetan macaques in a free-ranging group made physical contact with each other and formed huddling groups on the ledge of a steep cliff at night. We analyzed the size and composition of huddling groups and the frequencies of dyadic huddles—two individuals in physical contact—in the huddling group to determine the social influences on huddling behavior. Affiliated dyads that frequently groomed in the daytime frequently formed dyadic huddles in night-time huddling groups. Female–male dyads formed dyadic huddles less frequently than expected. In addition, Tibetan macaques chose 2 partners with which they initiated contact when they approached a huddling group. The frequencies with which some combinations of 3 individuals contacted each other and formed triangular huddles are not consistent with the expected frequencies. For example, female–male–male triads frequently formed triangular huddles in the birth season but did so infrequently in the mating season because of male competition for estrous females. When all 3 dyads within a certain triad formed dyadic huddles frequently, the triad was more likely to form a triangular huddle. The choices of approaching individuals might make a systematic, rather than random, positioning of individuals in huddling groups at their sleeping site.
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Huddling groups at sleeping sites, and allogrooming and proximity in the daytime during winter, were examined in a wild Japanese macaque (Macaca fuscata) troop on Kinkazan Island in the non-snowy district of northern Japan. All sleeping groups, defined as a cluster in which individuals huddle at sleeping sites, were formed on the ground. Their sizes tended to increase when the temperature was lower. The number of adults with mutual physical contact in sleeping groups increased when the size of sleeping groups increased. These results suggest that the physiological function of huddling is protection from low temperatures, and that macaques select the ground as sleeping sites to form large sized groups. Huddling was performed most frequently among kin dyads. Non-related dyads which appeared to be affiliative in the daytime also huddled frequently at sleeping sites. Even non-related dyads which showed affiliative behavior less frequently in the daytime exhibited huddling, at night, however, they did so less often than those of kin dyads and affiliated dyads. It appears that huddling at night by pairs that did not normally affiliate in the daytime was made possible by the increased tolerance of individuals responding to colder temperatures at night in winter. Furthermore, huddling, grooming, and proximity were exhibited at greater frequency between kin dyads, and between high-ranking males and specific females of kin groups, although the dyads of individuals older than 15 years often were involved only in huddling. These results suggest that two types of social bonds exist at sleeping sites in winter. One is the social bond common to both the daytime and nighttime, the other is peculiar to nighttime. Consequently, the social function of huddling is that, troop integration might increase at sleeping sites in winter as close social relationships among adults are extended more widely than those in daytime.
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