Effects of local habitat variation on the behavioral ecology of two sympatric groups of brown howler monkey (alouatta clamitans)

Although the brown howler monkey (Alouatta clamitans) is a relatively well-studied Neotropical primate, its behavioral and dietary flexibility at the intra-population level remains poorly documented. This study presents data collected on the behavior and ecology of two closely located groups of brown howlers during the same period at the RPPN Feliciano Miguel Abdala in southeastern Brazil. One group occupied a primary valley habitat, henceforth the Valley Group (VG), and the other group occupied a regenerating hillside habitat, the Hill Group (HG). We hypothesized differences in the behavior and ecological parameters between these sympatric groups due to the predicted harsher conditions on the hillside, compared to the valley. We measured several habitat parameters within the home range of both groups and collected data on the activity budget, diet and day range lengths, from August to November 2005, between dawn and dusk. In total, behavioral data were collected for 26 (318 h) and 28 (308 h) sampling days for VG and HG, respectively. As we predicted, HG spent significantly more time feeding and consumed less fruit and more leaves than VG, consistent with our finding that the hillside habitat was of lower quality. However, HG also spent less time resting and more time travelling than VG, suggesting that the monkeys had to expend more time and energy to obtain high-energy foods, such as fruits and flowers that were more widely spaced in their hill habitat. Our results revealed that different locations in this forest vary in quality and raise the question of how different groups secure their home ranges. Fine-grained comparisons such as this are important to prioritize conservation and management areas within a reserve

Genetic Diversity and Population History of a Critically Endangered Primate, the Northern Muriqui (Brachyteles hypoxanthus)

Social, ecological, and historical processes affect the genetic structure of primate populations, and therefore have key implications for the conservation of endangered species. The northern muriqui (Brachyteles hypoxanthus) is a critically endangered New World monkey and a flagship species for the conservation of the Atlantic Forest hotspot. Yet, like other neotropical primates, little is known about its population history and the genetic structure of remnant populations. We analyzed the mitochondrial DNA control region of 152 northern muriquis, or 17.6% of the 864 northern muriquis from 8 of the 12 known extant populations and found no evidence of phylogeographic partitions or past population shrinkage/expansion. Bayesian and classic analyses show that this finding may be attributed to the joint contribution of female-biased dispersal, demographic stability, and a relatively large historic population size. Past population stability is consistent with a central Atlantic Forest Pleistocene refuge. In addition, the best scenario supported by an Approximate Bayesian Computation analysis, significant fixation indices (ΦST = 0.49, ΦCT = 0.24), and population-specific haplotypes, coupled with the extirpation of intermediate populations, are indicative of a recent geographic structuring of genetic diversity during the Holocene. Genetic diversity is higher in populations living in larger areas (>2,000 hectares), but it is remarkably low in the species overall (θ = 0.018). Three populations occurring in protected reserves and one fragmented population inhabiting private lands harbor 22 out of 23 haplotypes, most of which are population-exclusive, and therefore represent patchy repositories of the species' genetic diversity. We suggest that these populations be treated as discrete units for conservation management purposes

Sex differences in the movement patterns of free-ranging chimpanzees (Pan troglodytes schweinfurthii): foraging and border checking

Most social primates live in cohesive groups, so travel paths inevitably reflect compromise: decision processes of individuals are obscured. The fission-fusion social organisation of the chimpanzee, however, allows an individual’s movements to be investigated independently. We followed 15 chimpanzees (8 male and 7 female) through the relatively flat forest of Budongo, Uganda, plotting the path of each individual over periods of 1-3 days. Chimpanzee movement was parsed into phases ending with halts of more than 20 minutes, during which individuals fed, rested or engaged in social activities. Males, lactating or pregnant females, and sexually receptive females all travelled similar average distances between halts, at similar speeds, and along similarly direct beeline paths. Compared to lactating or pregnant females, males did travel for a significantly longer time each day and halted more often, but the most striking sex differences appeared in the organisation of movement phases into a day’s path. After a halt, males tended to continue in the same direction as before. Lactating or pregnant females showed no such strategy and often retraced the preceding phase, returning to previously visited food patches. We suggest that female chimpanzee movements approximate an optimal solution to feeding requirements, whereas the paths of males allow integration of foraging with territorial defence. The ‘continually moving forwards’ strategy of males enables them to monitor their territory boundaries – border checking – whilst foraging, generally avoiding the explicit boundary patrols observed at other chimpanzee study sites

Primate responses to changing environments in the anthropocene

Most primates have slow life-histories and long generation times. Because environmental change is occurring at an unprecedented rate, gene-based adaptations are unlikely to evolve fast enough to offer successful responses to these changes. The paper reviews the most common types of habitat/landscape alterations, the extent of human-primate interactions, and the impact of climate change. It demonstrates how understanding behavioural flexibility as a response to environmental change will be crucial to optimize conservation efforts by constructing informed management plans. Comparisons across species, space, and time can be used to draw generalizations about primate responses to environmental change while considering their behavioural flexibility

Effects of the Distribution of Female Primates on the Number of Males

The spatiotemporal distribution of females is thought to drive variation in mating systems, and hence plays a central role in understanding animal behavior, ecology and evolution. Previous research has focused on investigating the links between female spatiotemporal distribution and the number of males in haplorhine primates. However, important questions remain concerning the importance of spatial cohesion, the generality of the pattern across haplorhine and strepsirrhine primates, and the consistency of previous findings given phylogenetic uncertainty. To address these issues, we examined how the spatiotemporal distribution of females influences the number of males in primate groups using an expanded comparative dataset and recent advances in Bayesian phylogenetic and statistical methods. Specifically, we investigated the effect of female distributional factors (female number, spatial cohesion, estrous synchrony, breeding season duration and breeding seasonality) on the number of males in primate groups. Using Bayesian approaches to control for uncertainty in phylogeny and the model of trait evolution, we found that the number of females exerted a strong influence on the number of males in primate groups. In a multiple regression model that controlled for female number, we found support for temporal effects, particularly involving female estrous synchrony: the number of males increases when females are more synchronously receptive. Similarly, the number of males increases in species with shorter birth seasons, suggesting that greater breeding seasonality makes defense of females more difficult for male primates. When comparing primate suborders, we found only weak evidence for differences in traits between haplorhines and strepsirrhines, and including suborder in the statistical models did not affect our conclusions or give compelling evidence for different effects in haplorhines and strepsirrhines. Collectively, these results demonstrate that male monopolization is driven primarily by the number of females in groups, and secondarily by synchrony of female reproduction within groups

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

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

Male-Mediated Gene Flow in Patrilocal Primates

BACKGROUND: Many group-living species display strong sex biases in dispersal tendencies. However, gene flow mediated by apparently philopatric sex may still occur and potentially alters population structure. In our closest living evolutionary relatives, dispersal of adult males seems to be precluded by high levels of territoriality between males of different groups in chimpanzees, and has only been observed once in bonobos. Still, male-mediated gene flow might occur through rare events such as extra-group matings leading to extra-group paternity (EGP) and female secondary dispersal with offspring, but the extent of this gene flow has not yet been assessed. METHODOLOGY/PRINCIPAL FINDINGS: Using autosomal microsatellite genotyping of samples from multiple groups of wild western chimpanzees (Pan troglodytes verus) and bonobos (Pan paniscus), we found low genetic differentiation among groups for both males and females. Characterization of Y-chromosome microsatellites revealed levels of genetic differentiation between groups in bonobos almost as high as those reported previously in eastern chimpanzees, but lower levels of differentiation in western chimpanzees. By using simulations to evaluate the patterns of Y-chromosomal variation expected under realistic assumptions of group size, mutation rate and reproductive skew, we demonstrate that the observed presence of multiple and highly divergent Y-haplotypes within western chimpanzee and bonobo groups is best explained by successful male-mediated gene flow. CONCLUSIONS/SIGNIFICANCE: The similarity of inferred rates of male-mediated gene flow and published rates of EGP in western chimpanzees suggests this is the most likely mechanism of male-mediated gene flow in this subspecies. In bonobos more data are needed to refine the estimated rate of gene flow. Our findings suggest that dispersal patterns in these closely related species, and particularly for the chimpanzee subspecies, are more variable than previously appreciated. This is consistent with growing recognition of extensive behavioral variation in chimpanzees and bonobos

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