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

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

You Mate, I Mate: Macaque Females Synchronize Sex not Cycles

Extended female sexuality in species living in multimale-multifemale groups appears to enhance benefits from multiple males. Mating with many males, however, requires a low female monopolizability, which is affected by the spatiotemporal distribution of receptive females. Ovarian cycle synchrony potentially promotes overlapping receptivity if fertile and receptive periods are tightly linked. In primates, however, mating is often decoupled from hormonal control, hence reducing the need for synchronizing ovarian events. Here, we test the alternative hypothesis that females behaviorally coordinate their receptivity while simultaneously investigating ovarian cycle synchrony in wild, seasonal Assamese macaques (Macaca assamensis), a promiscuous species with extremely extended female sexuality. Using fecal hormone analysis to assess ovarian activity we show that fertile phases are randomly distributed, and that dyadic spatial proximity does not affect their distribution. We present evidence for mating synchrony, i.e., the occurrence of the females' receptivity was significantly associated with the proportion of other females mating on a given day. Our results suggest social facilitation of mating synchrony, which explains (i) the high number of simultaneously receptive females, and (ii) the low male mating skew in this species. Active mating synchronization may serve to enhance the benefits of extended female sexuality, and may proximately explain its patterning and maintenance

Individual Facial Coloration in Male Eulemur fulvus rufus: A Condition-dependent Ornament?

Researchers studying individual variation in conspicuous skin coloration in primates have suggested that color indicates male quality. Although primate fur color can also be flamboyant, the potential condition dependence and thus signaling function of fur remains poorly studied. We studied sources of variation in sexually dichromatic facial hair coloration in red-fronted lemurs (Eulemur fulvus rufus). We collected data on 13 adult males in Kirindy Forest, Madagascar, during two study periods in 2006 and 2007, to determine whether variation in facial hair coloration correlates with male age, rank, androgen status, and reproductive success. We quantified facial hair coloration via standardized digital photographs of each male, assessed androgen status using fecal hormone measurements, and obtained data on reproductive success through genetic paternity analyses. Male facial hair coloration showed high individual variation, and baseline coloration was related to individual androgen status but not to any other parameter tested. Color did not reflect rapid androgen changes during the mating season. However, pronounced long-term changes in androgen levels between years were accompanied by changes in facial hair coloration. Our data suggest that facial hair coloration in red-fronted lemur males is under proximate control of androgens and may provide some information about male quality, but it does not correlate with dominance rank or male reproductive success

Reproductive and Life History Parameters of Wild Female Macaca assamensis

Information on basic reproductive parameters and life-history traits is crucial for the understanding of primate evolution, ecology, social behavior, and reproductive strategies. Here, we report 4 yr of data on reproductive and life-history traits for wild female Assamese macaques (Macaca assamensis) at Phu Khieo Wildlife Sanctuary, northeastern Thailand. During 2 consecutive reproductive seasons, we investigated reproductive behavior and sexual swelling size in 16 females and collected 1832 fecal samples. Using enzyme immunoassays, we measured fecal estrogen and progesterone metabolites to assess ovarian activity and timing of ovulation and to ascertain conceptions and pregnancies. Timing of reproduction was strictly seasonal (births: April–July, 86% in April–June, 4 yr, n = 29; conceptions: October–February, 65% in December–January, 2 yr, n = 17). Females showed no cyclic ovarian activity outside the mating season and conceived in their first or second cycle (mean: 1.2 cycles to conception, n = 13). Gestation length was on average 164.2 d (range: 158–170, n = 10), and females had their first infant at an age of 5 yr (n = 4). Interbirth intervals were bimodally distributed, with females giving birth on average every 13.9 or 23.2 mo. Shorter interbirth intervals were linked to early parturition within the birth season. Most females displayed subcaudal sexual swellings which, however, did not reliably indicate female reproductive status or fertility. Overall, our results fall within the range of findings reported for other macaque species. These results thus add to the growing body of information available for wild macaques, facilitating comparative studies for a better understanding of interspecific differences in social and reproductive patterns

Low levels of fruit nitrogen as drivers for the evolution of Madagascar's primate communities

The uneven representation of frugivorous mammals and birds across tropical regions – high in the New World, low in Madagascar and intermediate in Africa and Asia – represents a long-standing enigma in ecology. Several hypotheses have been proposed to explain these differences but the ultimate drivers remain unclear. Here, we tested the hypothesis that fruits in Madagascar contain insufficient nitrogen to meet primate metabolic requirements, thus constraining the evolution of frugivory. We performed a global analysis of nitrogen in fruits consumed by primates, as collated from 79 studies. Our results showed that average frugivory among lemur communities was lower compared to New World and Asian-African primate communities. Fruits in Madagascar contain lower average nitrogen than those in the New World and Old World. Nitrogen content in the overall diets of primate species did not differ significantly between major taxonomic radiations. There is no relationship between fruit protein and the degree of frugivory among primates either globally or within regions, with the exception of Madagascar. This suggests that low protein availability in fruits influences current lemur communities to select for protein from other sources, whereas in the New World and Old World other factors are more significant in shaping primate communities

Low Levels of Fruit Nitrogen as Drivers for the Evolution of Madagascar's Primate Communities

The uneven representation of frugivorous mammals and birds across tropical regions - high in the New World, low in Madagascar and intermediate in Africa and Asia - represents a long-standing enigma in ecology. Several hypotheses have been proposed to explain these differences but the ultimate drivers remain unclear. Here, we tested the hypothesis that fruits in Madagascar contain insufficient nitrogen to meet primate metabolic requirements, thus constraining the evolution of frugivory. We performed a global analysis of nitrogen in fruits consumed by primates, as collated from 79 studies. Our results showed that average frugivory among lemur communities was lower compared to New World and Asian-African primate communities. Fruits in Madagascar contain lower average nitrogen than those in the New World and Old World. Nitrogen content in the overall diets of primate species did not differ significantly between major taxonomic radiations. There is no relationship between fruit protein and the degree of frugivory among primates either globally or within regions, with the exception of Madagascar. This suggests that low protein availability in fruits influences current lemur communities to select for protein from other sources, whereas in the New World and Old World other factors are more significant in shaping primate communities

Characterization and social correlates of fecal testosterone and cortisol excretion in wild male Saguinus mystax

Reproductive success in male primates can be influenced by testosterone (T) and cortisol (C). We examined them in wild Saguinus mystax via fecal hormone analysis. Firstly, we wanted to characterize male hormonal status over the course of the year. Further we tested the influence of the reproductive status of the breeding female, social instability, and intergroup encounter rates on T levels, comparing the results with predictions of the challenge hypothesis (Wingfield et al., 1990). We also tested for interindividual differences in hormonal levels, possibly related to social or breeding status. We collected data during a 12-mo study on 2 groups of moustached tamarins at the Estación Biológica Quebrada Blanco in northeastern Peru. We found fairly similar T and C levels over the course of the year for all males. Yet an elevation of T shortly after the birth of infants, during the phase of ovarian inactivity of the group’s breeding female, was evident. Hormonal levels were not significantly elevated during a phase of social instability, did not correlate with intergroup encounter rates, and did not differ between breeding and nonbreeding males. Our results confirm the challenge hypothesis (Wingfield et al., 1990). The data suggest that reproductive competition inmoustached tamarins is not based on endocrinological, but instead on behavioral mechanisms, possibly combined with sperm competition.Deutsche Forschungsgemeinschaft (HE 1870/10-1,2

Mate-guarding constrains feeding activity but not energetic status of wild male long-tailed macaques (Macaca fascicularis).

Mate-guarding is an important determinant of male reproductive success in a number of species. Little is known however about the constraints of this behaviour, e.g. the associated energetic costs. We investigated these costs in long-tailed macaques where alpha males mate guard females to a lesser extent than predicted by the priority of access model. The study was carried out during two mating periods on three wild groups living in the Gunung Leuser National Park, Indonesia. We combined behavioural observations on males' locomotion and feeding activity, GPS records of distance travelled and non-invasive measurements of urinary C-peptide (UCP), a physiological indicator of male energetic status. Mate-guarding led to a decrease in feeding time and fruit consumption suggesting a reduced intake of energy. At the same time, vertical locomotion was reduced, which potentially saved energy. These findings, together with the fact that we did not find an effect of mate-guarding on UCP levels, suggest that energy intake and expenditure was balanced during mate-guarding in our study males. Mate-guarding thus seems to not be energetically costly under all circumstances. Given that in strictly seasonal rhesus macaques, high-ranking males lose physical condition over the mating period, we hypothesise that the energetic costs of mate-guarding vary inter-specifically depending on the degree of seasonality and that males of non-strictly seasonal species might be better adapted to maintain balanced energetic condition year-round. Finally, our results illustrate the importance of combining behavioural assessments of both energy intake and expenditure with physiological measures when investigating energetic costs of behavioural strategies