American Journal of Primatology最新文献

Olfactory behaviors serve a wide variety of social functions in mammals. Odor may signal information about attributes of individuals important for mating and reproduction. Olfactory behaviors, such as scent-marking, may also function as part of home range or resource defense strategies. We assessed the potential social and home range defense functions of olfactory behavior in a pair-living and sexually monogamous primate, Azara's owl monkey (Aotus azarae), in the Argentinian Chaco. This is the most extensive investigation of owl monkey olfactory behaviors in the wild. Individuals regularly performed olfactory behaviors (group mean + SD = 1.3 + 0.5 per hour). The patterns were generally comparable to those observed in studies of captive owl monkeys, except that urine washing was the most common behavior in the wild, as opposed to scent-marking and genital inspections. Most olfactory behaviors were performed by adults, and there were striking sex differences in genital inspections: almost all consisted of an adult male inspecting the paired adult female. These findings suggest that olfactory behaviors play an important role in signaling and coordinating reproduction among owl monkeys, particularly during periods of female conception and pregnancy. Additionally, our research indicates that these behaviors may also serve as a defense strategy for maintaining the core area of their home ranges. This study offers the first assessment of the role of olfactory behaviors in reproductive contexts and home range defense in pair-living, monogamous platyrrhine primates.

Despite decades of field study, very little is known about the molecular ecology of gibbons, particularly as it relates to their ability to disperse across degraded and fragmentary landscapes. The critically endangered western black crested gibbon (Nomascus concolor) has been reduced to a small, fragmented population with about 1300 individuals. In the largest population genetic study of free-ranging gibbons to date, we sampled 47 of these gibbons from 13 sites in China and generated 15 polymorphic autosomal microsatellite markers. We identify three population clusters of N. concolor in Yunnan centered in 1) the Wuliang and Ailao Mountains, 2) the Yongde Daxueshan Mountains, and 3) an isolated remnant near the border with Vietnam. Within the Wuliang Mountains, we identified four subclusters, three of which are bounded by high-altitude rhododendron forest, and one that is isolated from the main population by ~2 km of degraded forest and pasture. Least-cost path analysis and isolation by resistance modeling demonstrates that the population genetic distances among gibbons in Wuliangshan National Nature Reserve are significantly correlated with geographic paths that avoid use of high-altitude rhododendron forest in favor of evergreen broadleaf forest. Although these gibbons have likely undergone reductions in heterozygosity from recent consanguineous mating, we suggest that their active avoidance of inbreeding on the population level maintains higher than expected levels of genetic diversity. This research provides new insights into how gibbons interact with heterogeneous environments and expands our understanding of their molecular ecology and conservation genetics.

Changes in the rate of self-directed behavior—a proxy for social tension—offer valuable insights into individuals' experiences of social interactions. Many studies have tested the tension-reduction hypothesis, whereby grooming is expected to reduce social tension in the grooming partners. However, it is still unclear whether responses to grooming are affected by social factors such as an individual's role or social relationship with their partner, and whether responses are similar for females and males. Focussing on same-sex grooming in Yakushima Japanese macaques (Macaca fuscata yakui), we analyzed the effects of two social factors on the change in the rate of self-scratching after receiving grooming: sitting in contact with their partner outside of grooming contexts (as a measure of relationship strength) and rank distance. We collected 10-min postgrooming and matched-control focal samples on recipients of grooming. After controlling for postinhibitory rebound effects, grooming reduced scratching in females (suggesting that grooming was relaxing for the receiver), but not in males. In females, this reduction was associated with increased sitting in contact and increased rank distance: being groomed was more tension-reducing if the grooming partners spent time together outside of grooming contexts, or if their difference in rank was greater and therefore more conspicuous. The reduction effect was mediated by sitting in contact only when females had a higher-ranking—that is, more dominant and potentially aggressive—groomer. Our findings suggest that not all grooming interactions are perceived as equal, which has implications for its use as an index of relationship quality. To our knowledge, this represents the first study of postgrooming social tension in male Japanese macaques and our results highlight the need for caution when generalizing findings from only one sex to the species level.

The dietary ecology of a species can provide information on habitat requirements, food resources, and trophic interactions, important to guide conservation efforts of wildlife populations in endangered habitats. In this study, we investigated the dietary ecology of bearded capuchin monkeys (Sapajus libidinosus) in Brasilia National Park, in the endangered Cerrado biome of central Brazil. To obtain diet composition and evaluate the role of these primates as seed dispersers of local tree species, fecal sample collections and feeding observations were performed for a 7-month period. To determine whether seeds germinated better after passing through a primate gut, we conducted germination trials with (i) pulped seeds from trees, (ii) depulped seeds from trees, (iii) seeds from feces planted with feces, and (iv) seeds from feces planted without feces. During experimental procedures, 7308 seeds from 8 families and 10 species were planted. We found that S. libidinosus spent more time feeding on fruits than on any other food item and the diet consisted of 33 plant species from 21 families. However, 20% of their diet consisted of anthropic food. Most seeds planted with feces germinated faster compared to seeds in other experimental treatments, suggesting that passing through the gut and being deposited with fecal material is advantageous. The bearded capuchins also defecated many medium- (5 species) and large-sized (2 species) seeds that may be inaccessible to smaller arboreal frugivores. The results obtained emphasize the important role of bearded capuchins as seed dispersers for the maintenance and conservation of the endangered Cerrado biome.

Primates exhibit diverse social systems that are intricately linked to their biology, behavior, and evolution, all of which influence the acquisition and maintenance of their gut microbiomes (GMs). However, most studies of wild primate populations focus on taxa with relatively large group sizes, and few consider pair-living species. To address this gap, we investigate how a primate's social system interacts with key environmental, social, and genetic variables to shape the GM in pair-living, red-bellied lemurs (Eulemur rubriventer). Previous research on this species suggests that social interactions within groups influence interindividual microbiome similarity; however, the impacts of other nonsocial variables and their relative contributions to gut microbial variation remain unclear. We sequenced the 16S ribosomal RNA hypervariable V4–V5 region to characterize the GM from 26 genotyped individuals across 11 social groups residing in Ranomafana National Park, Madagascar. We estimated the degree to which sex, social group identity, genetic relatedness, dietary diversity, and home range proximity were associated with variation in the gut microbial communities residing in red-bellied lemurs. All variables except sex played a significant role in predicting GM composition. Our model had high levels of variance inflation, inhibiting our ability to determine which variables were most predictive of gut microbial composition. This inflation is likely due to red-bellied lemurs' pair-living, pair-bonded social system that leads to covariation among environmental, social, and genetic variables. Our findings highlight some of the factors that predict GM composition in a tightly bonded, pair-living species and identify variables that require further study. We propose that future primate microbiome studies should simultaneously consider environmental, social, and genetic factors to improve our understanding of the relationships among sociality, the microbiome, and primate ecology and evolution.

The Cayo Santiago rhesus macaque colony represents one of the most important nonhuman primate resources since their introduction to the Caribbean area in 1938. The 85 years of continuing existence along with the comprehensive database of the rhesus colony and the derived skeletal collections have provided and will continue to provide a powerful tool to test hypotheses about adaptive and evolutionary mechanisms in both biology and medicine.

Characterizing individual differences in cognition is crucial for understanding the evolution of cognition as well as to test the biological consequences of different cognitive traits. Here, we harnessed the strengths of a uniquely large, naturally-living primate population at the Cayo Santiago Biological Field Station to characterized individual differences in rhesus monkey performance across two social cognitive tasks. A total of n = 204 semi-free-ranging adult rhesus monkeys participated in a data collection procedure, where we aimed to test individuals on both tasks at two time-points that were one year apart. In the socioemotional responses task, we assessed monkeys' attention to conspecific photographs with neutral versus negative emotional expressions. We found that monkeys showed overall declines in interest in conspecific photographs with age, but relative increases in attention to threat stimuli specifically, and further that these responses exhibited long-term stability across repeated testing. In the gaze following task we assessed monkeys' propensity to co-orient with an experimenter. Here, we found no evidence for age-related change in responses, and responses showed only limited repeatability over time. Finally, we found some evidence for common individual variation for performance across the tasks: monkeys that showed greater interest in conspecific photographs were more likely to follow a human's gaze. These results show how studies of comparative cognitive development and aging can provide insights into the evolution of cognition, and identify core primate social cognitive traits that may be related across and within individuals.

Respiration is an invaluable signal that facilitates the real-time observation of physiological dynamics. In recent years, the advancement of noncontact measurement technology has gained momentum in capturing physiological activities in natural settings. This technology is anticipated to be found not only in humans but also in nonhuman primates. Currently, the predominant noncontact approach for nonhuman animals involves measuring vital signs through subtle variations in skin color. However, this approach is limited when addressing areas of the body covered with hair or when working in outdoor settings under fluctuating sunlight. To overcome this issue, we focused on noncontact respiratory measurements using millimeter-wave radar. Millimeter-wave radar systems, which employ millimeter waves that can penetrate animal fur and estimate respiration-derived periodic body motion, exhibit minimal susceptibility to sunlight interference. Thus, this method shows potential for conducting noncontact vital measurements in natural and outdoor settings. In this study, we validated a millimeter-wave radar methodology for capturing respiration in outdoor-housed rhesus macaques (Macaca mulatta). The radar was positioned beyond the captive enclosure and maintained at a distance >5 m from the target. Millimeter waves were transmitted to the target, and the reflected waves were used to estimate skin surface displacement associated with respiration. The results revealed periodic skin surface displacement, and the estimated respiratory rates weres within the reported range of respiratory rates for rhesus macaques. These results suggest the potential applicability of millimeter-wave radar for noncontact respiration monitoring in outdoor-living macaques without anesthesia or immobilization. The continued advancement of noncontact vital measurement technology will contribute to understanding primate mental and physical dynamics during their daily life.

Female dominance over males is more frequent in Malagasy lemurs than in other primate clades, but patterns of female–male dominance vary among species, and few data are available for one particularly species-rich genus, Lepilemur. We investigated the types, temporal distribution, and outcome of female–male agonistic conflicts in the Milne-Edwards' sportive lemur (Lepilemur edwardsi). Ten L. edwardsi belonging to five social units were equipped with radio collars and observed during 79 focal follows between May and November 1998. We quantified agonistic conflicts, monthly conflict rates, and documented the winner and context for all conflicts. Female–male agonistic conflicts (N = 162) occurred at a mean rate of 0.21 conflicts/hour within groups. Agonistic conflicts peaked during the birth season and occurred mostly in unknown or infant proximity contexts. Females won 96% of all decided agonistic conflicts (N = 154). Other outcomes occurred only when females were with infants during the birth season. In that context, one female sometimes withdrew from her pair partner, and another female withdrew or fled from an extra-group male whose attacks eventually led to infanticide. Our results suggest female dominance in pair-living L. edwardsi. We hypothesize that elevated female aggression may convey fitness benefits to female Lepilemur because it generally allows females to intervene quickly and efficiently on behalf of their infants against nonfather males who may approach the newborn infants when they are parked in vegetation.

Coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), was declared a pandemic by the World Health Organization in March 2020. Since then, viral spread from humans to animals has occurred worldwide. Nonhuman primates (NHPs) have been found to be susceptible to reverse-zoonosis transmission of SARS-CoV-2, but initial research suggested that platyrrhine primates are less susceptible than catarrhine primates. Here we report the natural SARS-CoV-2 infection of a common woolly monkey (Lagothrix lagothricha) from a wildlife rehabilitation center in Ecuador. The course of the disease, the eventual death of the specimen, and the pathological findings are described. Our results show the susceptibility of a new platyrrhine species to SARS-CoV-2 and provide evidence for the first time of a COVID-19-associated death in a naturally infected NHP. The putative route of transmission from humans, and implications for captive NHPs management, are also discussed. Given that common woolly monkeys are at risk of extinction in Ecuador, further understanding of the potential threat of SARS-CoV-2 to their health should be a conservation priority. A One Health approach is the best way to protect NHPs from a new virus in the same way that we would protect the human population.