Alpha male replacements and delayed dispersal in crested macaques (Macaca nigra).

In species with a high male reproductive skew, competition between males for the top dominant position is high and escalated fights are common between competitors. As a consequence, challenges incur potentially high costs. Selection should favor males who time an alpha male challenge to maximize chances of a successful outcome minimizing costs. Despite the importance of alpha male replacements for individual males, we know little about the timing of challenges and the condition of the challenger. We investigated the timing and process of alpha male replacements in a species living in multi-male groups with high male reproductive skew, the crested macaque. We studied four wild groups over 6 years in the Tangkoko Reserve, North Sulawesi, Indonesia, during which 16 alpha male replacements occurred. Although unusual for cercopithecines, male crested macaques delayed their natal dispersal until they attained maximum body mass and therefore fighting ability whereupon they emigrated and challenged the alpha male in another group. Accordingly, all observed alpha male replacements were from outside males. Ours is the first report of such a pattern in a primate species living in multi-male groups. Although the majority of alpha male replacements occurred through direct male-male challenges, many also took place opportunistically (i.e., after the alpha male had already been injured or had left the group). Furthermore, alpha male tenures were very short (averaging ca. 12 months). We hypothesize that this unusual pattern of alpha male replacements in crested macaques is related to the species-specific combination of high male reproductive skew with a large number of males per group. Am. J. Primatol. 79:e22448, 2017. © 2015 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.

Is social dispersal stressful? A study in male crested macaques (Macaca nigra).

In gregarious species, dispersal events represent one of the most dramatic changes in social life and environment an animal will experience during life due to increased predation risk, aggression from unfamiliar conspecifics and the lack of social support. However, little is known about how individuals respond physiologically to dispersal and whether this process is stressful for the individuals involved. We therefore studied the physiological stress response during dispersal in the crested macaque, a primate species in which males often change groups. Over a period of 14months and 14 dispersal events in 4 groups, we determined faecal glucocorticoid metabolite (FGCM) levels during the process of immigration into a new group and examined a variety of factors (e.g. male age, rank achieved, number of males in the group) potentially affecting FGCM levels during this process. We found that FGCM levels were significantly elevated in the first few days upon immigration, after which levels returned quickly to baseline. FGCM response levels upon immigration were significantly and positively influenced by the number of males in the group. The rank a male achieved upon immigration, aggression received, as well as the proximity to other males did not significantly influence FGCM levels. Our data confirm previous findings on other species demonstrating that in crested macaques immigration into a new social group is associated with an acute endocrine stress response. However, given that stress hormone levels remained elevated only for a short period of time, we do not expect males to experience high physiological costs during immigration. Given our limited knowledge on the physiological responses to dispersal in animals, this study contributes to our understanding of dispersal more generally, and particularly inter-individual differences in the stress response and the potential physiological costs associated with these.

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

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

Feeding behavior and aggression in wild Siberut macaques (Macaca siberu) living under low predation risk.

Investigating which factors influence feeding competition is crucial for our understanding of the diversity of social relationships. Socio-ecological models differ in their predictions whether predation risk directly influences feeding competition and which factors exactly predict contest competition. We investigated feeding competition in Siberut macaques (Macaca siberu), a species endemic to Siberut Island (West Sumatra, Indonesia). Siberut macaques experience low predation risk, as major predators (felids, raptors) are absent. They are therefore appropriate subjects to test the prediction that low predation risk reduces feeding competition. To estimate contest potential, we quantified size, spatial distribution and density of food plants, and the availability of alternative resources. We recorded behavior in food patches using a modified focal tree method. Food patches, sorted by decreasing average feeding group size, included large trees (40% of focal plant observations), lianas/strangler (16%), medium trees (9%), small (palm) trees (20%), and rattan (15%). Most food patches were clumped but occurred at low densities relative to the area of average group spread. Thus, availability of alternative food patches was low. Although food patch characteristics indicate high contest potential, the observed aggression rate (0.13 bouts between adults/h) was low relative to other primates. Average feeding group size was small relative to total group size, and feeding group size matched crown volume. Perceived predation risk was low, based on spatial and feeding behavior of juveniles. Together, these results suggest that predation risk may influence feeding competition. Social and temporal factors (patch feeding time), but not ecological factors (fruit abundance in patch and forest, alternative resources) predicted aggression frequency in food patches. Overall, comparative data are still relatively scarce, and researchers should collect more data on group spread, sub-grouping, perceived predation risk, and aggression in food patches before we can draw final conclusions about the role of predation risk for feeding competition.

Extra-pair paternity confirmed in wild white-handed gibbons.

Knowledge of the genetic mating system of animal species is essential for our understanding of the evolution of social systems and individual reproductive strategies. In recent years, genetic methods have uncovered an unexpected diversity of paternal genetic contributions across diverse animal social mating systems, but particularly in pair-living species. In most pair-living birds, for example, genetic and behavioral observations have confirmed a previously unknown significance of extra-pair copulations (EPCs) and extra-pair paternity. Among mammals, white-handed gibbons (Hylobates lar) are also known to live in pairs and are traditionally believed to be single-male single-female breeders. However, at Khao Yai National Park, Thailand, behavioral observations have confirmed the occurrence of both EPCs and functional multi-male grouping, but knowledge about the genetic mating system is still unavailable. In this study, we genotyped 89 white-handed gibbons of the Khao Yai population based on fecal samplings and were able to determine paternity for 41 offspring through short tandem repeat analysis. We found that females' stable social partners sired the majority (90.5%) of offspring (N = 38), while only a few (7.1%) offspring (n = 2 confirmed cases; n = 1 inferred case) were conceived with extra-pair partners. The paternity of one offspring remained inconclusive (2.4%), because the offspring's genotype did not mismatch with the genotypes of two potential sires. Like other predominantly pair-living species, gibbons appear to follow a mixed-reproductive strategy. The genetic mating system of wild white-handed gibbons is best described as flexible, primarily monogamous and opportunistically promiscuous. Inc.

Ecology of an endemic primate species (Macaca siberu) on Siberut Island, Indonesia.

Logging and forest loss continues to be a major problem within Southeast Asia and as a result, many species are becoming threatened or extinct. The present study provides the first detailed and comprehensive ecological data on the Siberut macaque (Macaca siberu), a primate species living exclusively on the island of Siberut off the west coast of Sumatra. Our results show that M. siberu is ecologically similar to its closest relative M. nemestrina occurring on the mainland, both species being semi-terrestrial, mainly frugivorous (75-76%), exhibit a large daily travel distance for their group size and spend more time on traveling than any other macaque species. The habitat of Siberut macaques was floristically very diverse (Simpson's index D=0.97), although somewhat impoverished in tree species richness, and had a lower tree basal area and a lower rattan density compared to other forests in Malesia (both rattan and palm tree fruit being an important food resource for Macaca siberu due to their long fruiting periods). These factors may lead to a lower diversity and abundance of fruit resources, and coupled with a high degree of frugivory of Siberut macaques, may explain the large amount of traveling observed in this species. The large home range requirements and strong dependence on fruit are important factors that need to be considered when developing conservation measures for this IUCN-listed (Category Vulnerable) species.

Social tolerance in wild female crested macaques (Macaca nigra) in Tangkoko-Batuangus Nature Reserve, Sulawesi, Indonesia.

In primates, females typically drive the evolution of the social system and present a wide diversity of social structures. To understand this diversity, it is necessary to document the consistency and/or flexibility of female social structures across and within species, contexts, and environments. Macaques (Macaca sp.) are an ideal taxon for such comparative study, showing both consistency and variation in their social relations. Their social styles, constituting robust sets of social traits, can be classified in four grades, from despotic to tolerant. However, tolerant species are still understudied, especially in the wild. To foster our understanding of tolerant societies and to assess the validity of the concept of social style, we studied female crested macaques, Macaca nigra, under entirely natural conditions. We assessed their degree of social tolerance by analyzing the frequency, intensity, and distribution of agonistic and affiliative behaviors, their dominance gradient, their bared-teeth display, and their level of conciliatory tendency. We also analyzed previously undocumented behavioral patterns in grade 4 macaques: reaction upon approach and distribution of affiliative behavior across partners. We compared the observed patterns to data from other populations of grade 4 macaques and from species of other grades. Overall, female crested macaques expressed a tolerant social style, with low intensity, frequently bidirectional, and reconciled conflicts. Dominance asymmetry was moderate, associated with an affiliative bared-teeth display. Females greatly tolerated one another in close proximity. The observed patterns matched the profile of other tolerant macaques and were outside the range of patterns of more despotic species. This study is the first comprehensive analysis of females' social behavior in a tolerant macaque species under natural conditions and as such, contributes to a better understanding of macaque societies. It also highlights the relevance of the social style concept in the assessment of the degree of tolerance/despotism in social systems.

Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar.

Although all macaques have a multimale multifemale mating system, the degree of promiscuity shown by the Barbary macaque is considered to be extreme in terms of both mating frequency and number of mating partners. How mating activity is distributed throughout the female menstrual cycle and whether or not copulations are concentrated around the fertile phase as in other members of the genus is, however, not known. To examine this, we collected data on rates of copulation throughout 29 ovarian cycles from 13 free-ranging females of the Gibraltar Barbary macaque population and related them to the time of ovulation and the female fertile phase as determined from fecal hormone analysis. In addition, patterns of male inspection of females and time spent in consortship, both indicators of female attractivity, were also analyzed. The results indicate that both mating behavior and female attractivity vary predictably with ovarian cycle stage. Rates of copulation were found to increase toward the time of ovulation, with a distinct peak of ejaculatory (but not non-ejaculatory) copulations occurring in the fertile phase. Additionally, we show that frequency of inspection of females by males and time spent in consortship were also highest during the fertile phase and that ejaculatory copulations and male pericopulatory behaviors were significantly correlated with levels of female sex hormones. Our findings indicate that the Barbary macaque shows a mating pattern during the cycle similar to that described for other members of the genus. More importantly, however, our study provides clear evidence that despite an extreme degree of promiscuity Barbary macaque males concentrate their reproductive effort to the fertile phase, implying that they are able to discern this period and that thus timing of ovulation is not concealed from them. Estrogen-related cues appear to be involved in the process of recognition of female reproductive status by males, but the exact nature of these cues and how male Barbary macaques use them remains to be clarified.

Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar.

Although female catarrhine primates show cyclic changes in sexual behavior and sexual swellings, the value of these sexual signals in providing information to males about timing of the fertile phase is largely unclear. Recently, we have shown that in Barbary macaques, males receive information from females which enables them to discern the fertile phase and to focus their reproductive effort accordingly. Here, we investigate the nature of the cues being used by examining female sexual behavior and the size of sexual swelling as potential indicators of the fertile phase. We collected behavioral data and quantified swelling size using digital images of 11 females of the Gibraltar Barbary macaque population and related the data to the time of ovulation and the fertile phase as determined from fecal hormone analysis. We found that rates of female sexual behaviors were not correlated with female estrogen levels and did not significantly differ between the fertile and non-fertile phases of the cycle. In contrast, swelling size was significantly correlated with female estrogen levels and increased predictably towards ovulation with size being maximal during the fertile phase. Moreover, frequencies of male ejaculatory copulations showed a strong positive correlation with swelling size and highest rates were found during maximum swelling. Our data provide strong evidence that female Barbary macaques honestly signal the probability of fertility through sexual swelling and that males apparently use this information to time their mating activities. Honest advertising of the fertile phase might be part of a female strategy to manipulate male mating behavior for their own advantage, such as ensure fertilization with high quality sperm or influence paternity outcome.

The impact of ecological variability on the reproductive endocrinology of wild female African elephants.

Non-invasive endocrine methods enable investigation of the relationship between ecological variation and ovarian activity and how this impacts on demographic processes. The underlying physiological factors driving high variation in inter-calving intervals among multi-parous African elephants offer an interesting system for such an investigation. This study investigates the relationship between Normalized Differential Vegetation Index (NDVI), an ecosystem surrogate measure of primary productivity, and fecal progestin concentrations among wild female elephants. Matched fecal samples and behavioral data on reproductive activity were collected from 37 focal individuals during the two-year study. Linear mixed models were used to explore the relationship between fecal 5alpha-pregnane-3-ol-20-one concentrations and the independent variables of NDVI, calf sex, female age, gestation day, and time since last parturition. Among both non-pregnant and pregnant females, fecal 5alpha-pregnane-3-ol-20-one concentrations were significantly correlated with time-specific NDVI indicating a strong relationship between ecological conditions and endocrine activity regulating reproduction. In addition, the age of a female and time since her last parturition impacted hormone concentrations. These results indicate that the identification of an individual's reproductive status from a single hormone sample is possible, but difficult to achieve in practice since numerous independent factors, particularly season, impact fecal hormone concentrations. Regardless of season, however, fecal 5alpha-pregnane-3-ol-20-one concentrations below 1 microg/g were exclusively collected from non-pregnant females, which could be used as a threshold value to identify non-pregnant individuals. Collectively the information generated contributes to a better understanding of environmental regulation of reproductive endocrinology in wild elephant populations, information salient to the management and manipulation of population dynamics in this species.

Physical, physiological, and behavioral correlates of musth in captive African elephants (Loxodonta africana).

Although musth in male African elephants (Loxodonta africana) is known to be associated with increased aggressiveness, urine dribbling (UD), temporal gland secretion (TGS), and elevated androgens, the temporal relationship between these changes has not been examined. Here, we describe the pattern of musth-related characteristics in 14 captive elephant bulls by combining long-term observations of physical and behavioral changes with physiological data on testicular and adrenal function. The length of musth periods was highly variable but according to our data set not related to age. Our data also confirm that musth is associated with elevated androgens and, in this respect, show that TGS and UD are downstream effects of this elevation, with TGS responding earlier and to lower androgen levels than UD. Because the majority of musth periods were associated with a decrease in glucocorticoid levels, our data also indicate that musth does not represent a physiological stress mediated by the hypothalamic-pituitary-adrenal axis. Furthermore, we demonstrate that the occurrence of musth is associated with increased aggression and that this is presumably androgen mediated because aggressive males had higher androgen levels. Collectively, the information generated contributes to a better understanding of what characterizes and initiates musth in captive African elephants and provides a basis for further studies designed to examine in more detail the factors regulating the intensity and duration of musth.

Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees.

Conspicuous swellings of the perineal skin can be observed in females of many catharrine primate species particularly during the middle stages of the ovarian cycle. The functional significance of this trait remains poorly understood. Recently, two hypotheses, the "reliable indicator" hypothesis and the "graded signal" hypothesis that take into account not only the pattern but also the exaggerated size of sexual swellings, have gained attention. Here we test several predictions made by these hypotheses by combining (i) direct size measures (from video captures) of female sexual swellings with (ii) urinary hormone data to indicate timing of ovulation through enzyme immunoassay measurements of estrone conjugates and pregnanediol glucuronide (PdG) and (iii) behavioral observations of male mating efforts throughout 36 ovulatory cycles in 12 wild chimpanzees. We are able to show that (i) even within the traditionally defined maximum swelling period, further slight increases in swelling size indicate approaching ovulation, and (ii) that male mating interest changes according to the changes in swelling size. Furthermore, absolute swelling size during the periovulatory period increases and the alpha male associates more with females as the number of cycles to conception decreases. Finally, when having the choice between several "maximally" tumescent females, the alpha male prefers the female that is in the fertile phase of her cycle rather than that with the biggest swelling at that time. Thus, most of our findings are in line with the predictions of the graded signal hypothesis while none of them would support the reliable indicator hypothesis.