Oliver Schülke

Dominance, aggression and physiological stress in wild male assamese macaques (Macaca Assamensis)

In group-living animals relative rank positions are often associated with differences in glucocorticoid output. During phases of social stability, when dominance positions are clear and unchallenged, subordinates often face higher costs in terms of social stress than dominant individuals. In this study we test this prediction and examine additional potential correlates of stress, such as reproductive season, age and amount of aggression received in wild, seasonally breeding Assamese macaques (Macaca assamensis). During a mating and a non-mating season we collected 394 h of focal observational data and 440 fecal samples of six adult and six large subadult males living in a multimale-multifemale group in their natural habitat in northeastern Thailand. The mating season was characterized by a general increase in aggressive behavior and glucocorticoid excretion across all males compared to the non-mating season. Among adult males, mating season glucocorticoid levels were significantly negatively related with dominance rank and positively with the amount of aggression received. Both relationships were non-significant among large subadult males. Thus, our results suggest that in adult Assamese macaques a high dominance position is not associated with high costs. Low costs of dominance might be induced by strong social bonds among top-ranking males, which exchange frequent affiliative interactions and serve as allies in coalitionary aggression against potentially rank-challenging subordinate males.

Female reproductive synchrony predicts skewed paternity across primates

Recent studies have uncovered remarkable variation in paternity within primate groups. To date, however, we lack a general understanding of the factors that drive variation in paternity skew among primate groups and across species. Our study focused on hypotheses from reproductive skew theory involving limited control and the use of paternity “concessions” by investigating how paternity covaries with the number of males, female estrous synchrony, and rates of extragroup paternity. In multivariate and phylogenetically controlled analyses of data from 27 studies on 19 species, we found strong support for a limited control skew model, with reproductive skew within groups declining as female reproductive synchrony and the number of males per group increase. Of these 2 variables, female reproductive synchrony explained more of the variation in paternity distributions. To test whether dominant males provide incentives to subordinates to resist matings by extragroup males, that is, whether dominants make concessions of paternity, we derived a novel prediction that skew is lower within groups when threat from outside the group exists. This prediction was not supported as a primary factor underlying patterns of reproductive skew among primate species. However, our approach revealed that if concessions occur in primates, they are most likely when female synchrony is low, as these conditions provide alpha male control of paternity that is assumed by concessions models. Collectively, our analyses demonstrate that aspects of male reproductive competition are the primary drivers of reproductive skew in primates.

Male competition and its hormonal correlates in Assamese macaques (Macaca assamensis)

In polygynous mammals, where males compete over access to females, the potential of males to monopolize reproductive females largely depends on the spatio-temporal distribution of reproductive females. We investigated mechanisms of male reproductive competition and its hormonal basis in a cercopithecine species with reduced contest potential owing to female reproductive synchrony and concealed ovulation. Over 16 months including two mating seasons we collected 1218 h of observational focal animal data and 1254 fecal samples of 11-12 adult and large subadult male Assamese macaques (Macaca assamensis) living in their natural habitat in Thailand. Androgen output along with aggressive behavior showed a seasonal pattern, with highest values being obtained by all males during the mating season and by those males experiencing acute social challenges, e.g. rank change and dispersal. Individual androgen levels and rates of attacks were linked across the study period, suggesting a promoting function of androgens for aggressive behavior. Dominance rank predicted neither mating success nor androgen levels consistently, indicating a reduced selective advantage of high social status for general mating access. However, high ranking males engaged in extended consortships with reproductive females. Distribution of consortships across males followed a priority of access distribution, with the two top ranking males accounting for 75% of consort activity, suggesting that high social status also carries fitness benefits in a species characterized by low contest potential.

Responses to social and environmental stress are attenuated by strong male bonds in wild macaques

Significance Male macaques form social bonds similar to human friendships that buffer them against day-to-day stressors. If male primates live in multimale groups they usually fight fiercely over access to females, but males can develop friendly relationships with a few group mates. The strength of these “friendships” has now been shown to buffer against the negative effects of social and environmental stressors, a phenomenon that was previously only described for females and pair-living animals. Long-term glucocorticoid (stress hormone) elevation can increase susceptibility to disease and mortality. This study shows that variation in everyday stressors such as the amount of aggression received or cold stress can cause such long-term elevated glucocorticoid levels but that keeping a few close male associates will avoid that. In humans and obligatory social animals, individuals with weak social ties experience negative health and fitness consequences. The social buffering hypothesis conceptualizes one possible mediating mechanism: During stressful situations the presence of close social partners buffers against the adverse effects of increased physiological stress levels. We tested this hypothesis using data on social (rate of aggression received) and environmental (low temperatures) stressors in wild male Barbary macaques (Macaca sylvanus) in Morocco. These males form strong, enduring, and equitable affiliative relationships similar to human friendships. We tested the effect of the strength of a male’s top three social bonds on his fecal glucocorticoid metabolite (fGCM) levels as a function of the stressors’ intensity. The attenuating effect of stronger social bonds on physiological stress increased both with increasing rates of aggression received and with decreasing minimum daily temperature. Ruling out thermoregulatory and immediate effects of social interactions on fGCM levels, our results indicate that male Barbary macaques employ a tend-and-befriend coping strategy in the face of increased environmental as well as social day-to-day stressors. This evidence of a stress-ameliorating effect of social bonding among males under natural conditions and beyond the mother–offspring, kin or pair bond broadens the generality of the social buffering hypothesis.

Concealed Fertility and Extended Female Sexuality in a Non-Human Primate (Macaca assamensis)

In numerous primates living in mixed-sex groups, females display probabilistic cues of fertility to simultaneously concentrate paternity to dominant males while diluting it amongst others as a means to reduce the risk of infanticide and to increase male care for offspring. A few species, however, lack these cues and potentially conceal fertility from males; yet, to date, little is known about mating patterns and their underlying proximate mechanisms in such species. Here, we investigated mating activity and sexual consortships relative to female reproductive state in wild Assamese macaques (Macaca assamensis), a species where females lack prominent anogenital swellings and copulation calls. During two mating seasons (2837 contact hours) we recorded sexual and social behaviors, sexual consortships, and collected 1178 fecal samples (n = 15 females) which were analyzed for progestogen concentrations to assess female reproductive state and to determine the timing of ovulation and conception. Although mostly conceiving in their first ovarian cycle, females were sexually receptive throughout the entire 4-month mating season, and within-cycle mating frequencies were not increased during fertile phases. Dominant males did not monopolize fertile matings, and consortships by high-ranking males lasted for long periods, which were not exclusively linked to female fertile phases. Furthermore, females copulated promiscuously but not randomly, i.e. for almost every female, matings were concentrated to a certain male, irrespective of male rank. Collectively, we demonstrate that fertility is undisclosed to males. The extreme extended female sexuality facilitated by concealed fertility may allow females to create differentiated mating relationships within a promiscuous mating system. Our study provides important new insight into the plasticity of female sexuality in non-human primates.

Coalition formation among Barbary macaque males: the influence of scramble competition

Owing to the nature of male competition over a nonshareable resource, cooperation and coalition formation are unexpected among mammalian males. Nevertheless, coalitions of unrelated males are widespread across mammals. Recently, a mathematical model for the evolution of male coalitions within groups was developed, predicting patterns and outcomes of coalitions depending on the degree of contest competition for mates. We tested this model in a species with presumably low-contest competition. Accordingly, under low contest, coalitions should be large, formed by mid- to low-ranking males targeting top-rankers and aimed at decreasing reproductive skew (all-up levelling coalitions). We also investigated the effect of scramble competition on coalitions, as its impact was not included in the model. Scramble competition is expected to be pronounced in our study population of Barbary macaques, Macaca sylvanus, and thus we predicted that coalitions should target mainly young immigrants, irrespective of rank, to isolate them and eventually reduce male group size and, consequently, scramble competition. Data on social interactions, including coalitions, were collected on 23 males of a group of Barbary macaques living at Affenberg Salem, Germany. Coalition size was small, coalitions rarely targeted top-ranking males and all-up levelling coalitions were rare. Overall, the model was not confirmed. In contrast, more than three-quarters of coalitions targeted young immigrants, which were isolated from the group. Thus, male coalition formation in our group seemed to be influenced by scramble rather than contest competition. Both modes of competition should thus be taken into account if payoffs of coalition formation are investigated.

Social Relationships in Free-Ranging Male Macaca arctoides

Macaque social relationships differ greatly between species. Based on captive studies that focus mainly on females, researchers have classified stumptail macaque (Macaca arctoides) social relationships as tolerant, as indicated by a high rate of affiliation, frequent aggression, and symmetrical conflicts. To accumulate more data on male social relationships, which are relatively understudied, and to generate comparative data, we investigated male social relationships in a provisioned group of 68 free-ranging, naturally dispersing stumptail macaques in southern Thailand. We collected continuous focal animal and ad libitum data on 7 adult and 2 subadult males, recording social behavior during 283 contact hours between December 2006 and March 2007. Stumptail macaques of this population were less tolerant than predicted based on previous studies on captive groups: Rates of spatial proximity, affiliation, and aggression were low, most males directed affiliative behavior toward higher-ranking males, and conflicts were generally of low intensity and relatively asymmetrical. Thus, male stumptail macaques of the focal group appear to differ in their social style from a previous study of a captive group that mainly comprised of females. In some traits, they are even more intolerant than rhesus macaques, an intensively studied intolerant macaque species. We also compare our data on stumptail macaque males to those on other male macaques, but available data are too sparse to draw final conclusions.

Stable heterosexual associations in a promiscuous primate

Close associations between adult males and females are rare among group-living, nonmonogamous mammals but may mark the transition from life in promiscuous bisexual groups to groups of pairs or pair living. Although heterosexual friendships have been described in baboons, these are short-term affairs serving as protection against infanticide and thus tightly linked to the presence of vulnerable infants. Long-term association may be adaptive in situations of low male monopolization potential where it pays to invest in a particular female partner instead of spreading the effort among many females. Using long-term data, we investigated maleefemale and maleeinfant associations in wild Assamese macaques, Macaca assamensis. Group-wide and individual maleefemale associations were stable for at least 2 or 3 years. Association during the mating season but not before the mating season predicted male mating success, lending support to the ‘friends with benefits’ but not the ‘mating effort’ hypothesis. Mating success in turn predicted maleefemale association at birth as well as maleeinfant association before weaning. In support of the ‘paternal care hypothesis’ paternity was an independent predictor of maleeinfant association beyond weaning age, creating potential for true paternal care. We thus postulate that particular demographic and life history circumstances may favour maleefemale friendships by creating a positive feedback between maleefemaleeinfant associations driven by paternal care and maleefemale associations promoted by increased mating access to drive the evolution of long-term maleefemale bonds.

The evolution of social bonds in primate males

Social bonds, here defined as strong, equitable and enduring social relationships, increase fitness in both male and female primates irrespective of their dispersal regime. Despite the benefits they carry for some, social bonds evolved more often among female than among male primates which is thought to be caused by the unsharable nature of males’ limiting resource, fertilizations. Here we present a structured review of variation in primate male social relationships, mating systems, and social organization. In addition to classical socio-ecological reasoning and recent models on the evolution of male coalitions, we consider the phylogenetic history of species living in multi-male groups and alternative evolutionary routes to male co-residency, which may constrain the evolution of male social bonds in some cases. We summarize our results in a conceptual framework that represents the effects of male contest competition within and between groups on male social organization, affiliation and cooperation. We conclude that male social bonds evolved as long-term alliances that gain their adaptive function in within group contests and, thus, that the evolution of male social bonds is driven by variation in within group contest competition. Between group contest competition may select for large male group size but in the end it is the narrow window of medium to low within group contest competition that promotes the evolution of political coalitions and thus is responsible for the rarity of social bonds among primate males.

Evolution of pair-living in Phaner furcifer

Pair-living evolved several times independently in the primate lineage and most likely for more than one reason. Currently, there are 7 hypotheses regarding the evolution of pair-living in primates. They may explain several but not all cases. I investigated the applicability of the explanations to fork-marked lemurs Phaner furcifer. I used information from a long-term study on 8 fork-marked lemur families in Kirindy Forest to evaluate the hypotheses. Fork-marked lemurs live in uniform dispersed pairs, which share and defend a territory but spend three-quarters of their activity time apart from each other. Unconditional female dominance and lack of permanent close association between pair-partners disqualify most hypotheses. Lack of male parental care and long travel distances in small home ranges disqualify other explanations. I conclude that there is no support a priori for any current pair-living hypothesis and that the newly formulated intersexual-feeding-competition hypothesis best explains the evolution of pair-living in fork-marked lemurs. Accordingly, female range exclusivity evolved first as a consequence of intense feeding competition. Subsequently, indirect feeding competition drove females to accept a single male to share their territory as a defense against feeding competition from males whose ranges unsystematically overlap those of several females. This situation led to pair-living because formation of dispersed one-male-multifemale-units was too costly for males in terms of reduced foraging efficiency.