Quantifying uncertainty due to fission-fusion dynamics as a component of social complexity.

Groups of animals (including humans) may show flexible grouping patterns, in which temporary aggregations or subgroups come together and split, changing composition over short temporal scales, (i.e. fission and fusion). A high degree of fission-fusion dynamics may constrain the regulation of social relationships, introducing uncertainty in interactions between group members. Here we use Shannon's entropy to quantify the predictability of subgroup composition for three species known to differ in the way their subgroups come together and split over time: spider monkeys (Ateles geoffroyi), chimpanzees (Pan troglodytes) and geladas (Theropithecus gelada). We formulate a random expectation of entropy that considers subgroup size variation and sample size, against which the observed entropy in subgroup composition can be compared. Using the theory of set partitioning, we also develop a method to estimate the number of subgroups that the group is likely to be divided into, based on the composition and size of single focal subgroups. Our results indicate that Shannon's entropy and the estimated number of subgroups present at a given time provide quantitative metrics of uncertainty in the social environment (within which social relationships must be regulated) for groups with different degrees of fission-fusion dynamics. These metrics also represent an indirect quantification of the cognitive challenges posed by socially dynamic environments. Overall, our novel methodological approach provides new insight for understanding the evolution of social complexity and the mechanisms to cope with the uncertainty that results from fission-fusion dynamics

Maternal Condition Does Not Influence Birth Sex Ratios in Anubis Baboons (Papio anubis)

Trivers and Willard predicted that when parental condition has differential effects on the fitness of male and female offspring, parents who are in good condition will bias investment toward the sex that benefits most from additional investment. Efforts to test predictions derived from Trivers and Willard's model have had mixed results, perhaps because most studies have relied on proxy measures of parental condition, such as dominance rank. Here, we examine the effects of female baboons condition on birth sex ratios and post-natal investment, based on visual assessments of maternal body condition. We find that local environmental conditions have significant effects on female condition, but maternal condition at conception has no consistent relationship with birth sex ratios. Mothers who are in poorer condition at the time of conception resume cycling significantly later than females who are in better condition, but the sex of their infants has no effect on the time to resumption of cycling. Thus, our findings provide strong evidence that maternal condition influences females' ability to reproduce, but females do not facultatively adjust the sex ratio of their offspring in relation to their dominance rank or current condition

Paternity alone does not predict long-term investment in juveniles by male baboons

Adult male chacma baboons (Papio hamadryas ursinus) form preferential associations, or friendships, with particular lactating females. Males exhibit high levels of affiliative contact with their friends’ infants and defend them from potentially infanticidal attacks (Palombit et al. 1997). Little is known about males’ associations with juveniles once they have passed the period of infanticidal risk. We conducted an observational, experimental, and genetic study of adult male and juvenile chacma baboons in the Moremi Reserve, Botswana. We identified preferential associations between males and juveniles and used behavioral data and a playback experiment to explore whether those associations have potential fitness benefits for juveniles. We determined whether males preferentially invest in care of their own offspring. We also determined how often males invest in care of their former friends’ offspring. The majority of juveniles exhibited preferential associations with one or two males, who had almost always been their mother’s friend during infancy. However, in only a subset of these relationships was the male the actual father, in part because many fathers died or disappeared before their offspring were weaned. Male caretakers intervened on behalf of their juvenile associates in social conflicts more often than they intervened on behalf of unconnected juveniles, and they did not appear to differentiate between genetic offspring and unrelated associates. Playbacks of juveniles’ distress calls elicited a stronger response from their caretakers than from control males. Chacma males may provide care to unrelated offspring of former friends because the costs associated with such care are low compared with the potentially high fitness costs of refusing aid to a juvenile who is a possible offspring

Methodological considerations in the analysis of fecal glucocorticoid metabolites in tufted capuchins (Cebus apella)

Analysis of fecal glucocorticoid (GC) metabolites has recently become the standard method to monitor adrenocortical activity in primates noninvasively. However, given variation in the production, metabolism, and excretion of GCs across species and even between sexes, there are no standard methods that are universally applicable. In particular, it is important to validate assays intended to measure GC production, test extraction and storage procedures, and consider the time course of GC metabolite excretion relative to the production and circulation of the native hormones. This study examines these four methodological aspects of fecal GC metabolite analysis in tufted capuchins (Cebus apella). Specifically, we conducted an adrenocorticotrophic hormone (ACTH) challenge on one male and one female capuchin to test the validity of four GC enzyme immunoassays (EIAs) and document the time course characterizing GC me- tabolite excretion in this species. In addition, we compare a common field-friendly technique for extracting fecal GC metabolites to an established laboratory extraction methodology and test for effects of storing “field extracts” for up to 1 yr. Results suggest that a corticosterone EIA is most sensitive to changes in GC production, provides reliable measures when extracted according to the field method, and measures GC metabolites which remain highly stable after even 12 mo of storage. Further, the time course of GC metabolite excretion is shorter than that described yet for any primate taxa. These results provide guidelines for studies of GCs in tufted capuchins, and underscore the importance of validating methods for fecal hormone analysis for each species of interest

Ape Conservation Physiology: Fecal Glucocorticoid Responses in Wild Pongo pygmaeus morio following Human Visitation

Nature-based tourism can generate important revenue to support conservation of biodiversity. However, constant exposure to tourists and subsequent chronic activation of stress responses can produce pathological effects, including impaired cognition, growth, reproduction, and immunity in the same animals we are interested in protecting. Utilizing fecal samples (N = 53) from 2 wild habituated orangutans (Pongo pygmaeus morio) (in addition to 26 fecal samples from 4 wild unhabituated orangutans) in the Lower Kinabatangan Wildlife Sanctuary of Sabah, Malaysian Borneo, we predicted that i) fecal glucocorticoid metabolite concentrations would be elevated on the day after tourist visitation (indicative of normal stress response to exposure to tourists on the previous day) compared to samples taken before or during tourist visitation in wild, habituated orangutans, and ii) that samples collected from habituated animals would have lower fecal glucocorticoid metabolites than unhabituated animals not used for tourism. Among the habituated animals used for tourism, fecal glucocorticoid metabolite levels were significantly elevated in samples collected the day after tourist visitation (indicative of elevated cortisol production on the previous day during tourist visitation). Fecal glucocorticoid metabolite levels were also lower in the habituated animals compared to their age-matched unhabituated counterparts. We conclude that the habituated animals used for this singular ecotourism project are not chronically stressed, unlike other species/populations with documented permanent alterations in stress responses. Animal temperament, species, the presence of coping/escape mechanisms, social confounders, and variation in amount of tourism may explain differences among previous experiments. Acute alterations in glucocorticoid measures in wildlife exposed to tourism must be interpreted conservatively. While permanently altered stress responses can be detrimental, preliminary results in these wild habituated orangutans suggest that low levels of predictable disturbance can likely result in low physiological impact on these animals

Matrilineal behavioral and physiological changes following the death of a non-alpha matriarch in rhesus macaque

In many species, the loss of alpha matriarchs is associated with a number of negative outcomes such as troop fission, eviction, wounding, and reduced vitality. However, whether the dramatic consequences of their loss are due to their role as an old experienced figure or to their alpha status remains unclear. In a retrospective study, we tested that in a semi-free ranging colony of rhesus macaques (Macaca mulatta), the removal of a non-alpha matriarch, who had a large set of kin, led to changes in behavior and physiological stress within her matriline. Following her removal, her matriline increased in aggression, vigilance, and social grooming. Additionally, hierarchical stability, measured by levels of rank changes, decreased within her matriline, and levels of intense aggression by high-ranking animals were more frequent, as well as matrilineal wounding. Although ordinal rank was positively associated with higher chronic hair cortisol concentrations (HCCs) in the months before the matriarch’s removal, following her removal, only those who experienced large increases in rank within her matriline displayed higher HCCs. Changes in matrilineal stability, aggression, behavior, and HCCs within the other two matrilines in the troop were not evident, although caution is needed due to the small sample sizes. We conclude that the removal of the non-alpha matriarch led to matrilineal instability, characterized by higher levels of aggression and subsequent vigilance, rank changes, physiological stress, and grooming. We suggest that non-alpha matriarchs with a large number of kin and social support can be integral to the stability of matrilines.Division of Intramural Research, National Institute of Child Health and Human Development, 1ZIAHD001107- 3

Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus)

Intense reproductive competition and social instability are assumed to increase concentrations of glucocorticoids and androgens in vertebrates, as a means of coping with these challenges. In seasonally breeding redfronted lemurs (Eulemur fulvus rufus), the mating and the birth season and the associated increased male competition are predicted to pose such reproductive challenges. In this paper, we investigate seasonal variation in hormone excretion in male redfronted lemurs, and examine whether this variation is associated with social or ecological factors. Although dominance status has been shown to affect individual stress levels across many taxa, we predicted no rank-related differences in glucocorticoids for redfronted lemurs because relatively equal costs are associated with both high and low rank positions (based on patterns of rank acquisition/maintenance and threats toward subordinates). Over a 14-month period, we collected behavioral data (1843 focal hours) and 617 fecal samples from 13 redfronted lemur males in Kirindy Forest/Madagascar. We found no general rank-related pattern of testosterone or glucocorticoid excretion in this species. Both hormones were excreted at significantly higher levels during the mating and the birth season, despite social stability during both periods. The elevated mating season levels may be explained by increased within-group reproductive competition during this time and are in line with previous studies of other seasonally reproducing primates. For the birth season increase, we propose that the predictable risk of infanticide in this highly seasonal species affects male gonadal and adrenal endocrine activity. We evaluate alternative social and ecological factors influencing the production of both hormone classes and conclude based on our preliminary investigations that none of them can account for the observed pattern

Low Frequency Groans Indicate Larger and More Dominant Fallow Deer (Dama dama) Males

Background: Models of honest advertisement predict that sexually selected calls should signal male quality. In most vertebrates, high quality males have larger body sizes that determine higher social status and in turn higher reproductive success. Previous research has emphasised the importance of vocal tract resonances or formant frequencies of calls as cues to body size in mammals. However, the role of the acoustic features of vocalisations as cues to other quality-related phenotypic characteristics of callers has rarely been investigated. Methodology/Principal Findings: We examined whether the acoustic structure of fallow deer groans provides reliable information on the quality of the caller, by exploring the relationships between male quality (body size, dominance rank, and mating success) and the frequency components of calls (fundamental frequency, formant frequencies, and formant dispersion). We found that body size was not related to the fundamental frequency of groans, whereas larger males produced groans with lower formant frequencies and lower formant dispersion. Groans of high-ranking males were characterised by lower minimum fundamental frequencies and to a lesser extent, by lower formant dispersions. Dominance rank was the factor most strongly related to mating success, with higher-ranking males having higher mating success. The minimum fundamental frequency and the minimum formant dispersion were indirectly related to male mating success (through dominance rank). Conclusion/Significance: Our study is the first to show that sexually selected vocalisations can signal social dominance in mammals other than primates, and reveals that independent acoustic components encode accurate information on different phenotypic aspects of male quality

Female chacma baboons form strong, equitable, and enduring social bonds

Analyses of the pattern of associations, social interactions, coalitions, and aggression among chacma baboons (Papio hamadryas ursinus) in the Okavango Delta of Botswana over a 16-year period indicate that adult females form close, equitable, supportive, and enduring social relationships. They show strong and stable preferences for close kin, particularly their own mothers and daughters. Females also form strong attachments to unrelated females who are close to their own age and who are likely to be paternal half-sisters. Although absolute rates of aggression among kin are as high as rates of aggression among nonkin, females are more tolerant of close relatives than they are of others with whom they have comparable amounts of contact. These findings complement previous work which indicates that the strength of social bonds enhances the fitness of females in this population and support findings about the structure and function of social bonds in other primate groups

Stereotypic head twirls, but not pacing, are related to a ‘pessimistic’-like judgment bias among captive tufted capuchins (Cebus apella)

Abnormal stereotypic behaviour is widespread among captive non-human primates and is generally associated with jeopardized well-being. However, attributing the same significance to all of these repetitive, unvarying and apparently functionless behaviours may be misleading, as some behaviours may be better indicators of stress than others. Previous studies have demonstrated that the affective state of the individual can be inferred from its bias in appraising neutral stimuli in its environment. Therefore, in the present study, in order to assess the emotional state of stereotyping individuals, 16 captive tufted capuchins (Cebus apella) were tested on a judgment bias paradigm and their faecal corticoid levels were measured in order to assess the intensity of the emotional state. Capuchins with higher levels of stereotypic head twirls exhibited a negative bias while judging ambiguous stimuli and had higher levels of faecal corticoids compared to subjects with lower levels of head twirls. Levels of stereotypic pacing, however, were not correlated with the monkeys’ emotional state. This study is the first to reveal a positive correlation between levels of stereotypic behaviour and a ‘pessimistic’-like judgment bias in a non-human primate by employing a recently developed cognitive approach. Combining cognitive tests that evaluate the animals’ affective valence (positive or negative) with hormonal measurements that provide information on the strength of the emotional state conduces to a better understanding of the animals’ affective state and therefore to their well-being