The marmoset is a fundamental nonhuman primate model for the study of aging, neurobiology, and many other topics. Genetic management of captive marmoset colonies is complicated by frequent chimerism in the blood and other tissues, a lack of tools to enable cost-effective, genome-wide interrogation of variation, and historic mergers and migrations of animals between colonies. We implemented genotype-by-sequencing (GBS) of hair follicle derived DNA (a minimally chimeric DNA source) of 82 marmosets housed at the Southwest National Primate Research Center (SNPRC). Our primary goals were the genetic characterization of our marmoset population for pedigree verification and colony management and to inform the scientific community of the functional genetic makeup of this valuable resource. We used the GBS data to reconstruct the genetic legacy of recent mergers between colonies, to identify genetically related animals whose relationships were previously unknown due to incomplete pedigree information, and to show that animals in the SNPRC colony appear to exhibit low levels of inbreeding. Of the >99,000 single-nucleotide variants (SNVs) that we characterized, >9800 are located within gene regions known to harbor pathogenic variants of clinical significance in humans. Overall, we show the combination of low-resolution (sparse) genotyping using hair follicle DNA is a powerful strategy for the genetic management of captive marmoset colonies and for identifying potential SNVs for the development of biomedical research models.
Black-and-white snub-nosed monkeys (Rhinopithecus bieti) rely on behavioral and dietary flexibility to survive in temperate latitudes at high-elevation habitats characterized by climate and resource seasonality. However, little is known about how elevation influences their behavioral and dietary flexibility at monthly or seasonal scales. We studied an isolated R. bieti population at Mt. Lasha in the Yunling Provincial Nature Reserve, Yunnan, China, between May 2008 and August 2016 to assess the impacts of elevation on feeding behavior and diet. Across our sample, R. bieti occupied elevations between 3031 and 3637 m above mean sea level (amsl), with a 315.1 m amsl range across months and a 247.3 m amsl range across seasons. Contrary to expectations, individuals spent less time feeding when ranging across higher elevations. Lichen consumption correlated with elevation use across months and seasons, with individuals spending more time feeding on this important resource at higher elevations. Leaf consumption only correlated with elevation use during the spring. Our results suggest that R. bieti do not maximize their food intake at higher elevations and that monthly and seasonal changes in lichen and leaf consumption largely explain variation in elevation use. These findings shed light on the responses of R. bieti to environmental change and offer insight into strategies for conserving their habitats in the face of anthropogenic disturbance.
Nonhuman primate species currently face human-induced pressures and will continue to face them in the modern landscape. These pressures require conservation projects in primate habitat countries to aid in protection, preservation, and conservation. Though there are several examples of primate conservation projects, starting up an initiative can be a daunting task. The American Society of Primatology (ASP) Conservation Committee hosted a video webinar presenting on the first steps of developing, running and continuing a primate conservation program. Dr. Christopher Shaffer, Rahayu Oktaviani, and Dr. Jill Pruetz presented their early program experiences establishing wild primate conservation projects to educate primatologists around the world. The running themes of the presentations included establishing community, working locally, impacting locally and preparing for the future.
Gibbons (Hylobatidae) are the smallest of the apes, known for their arboreal behavior and stereotyped songs. These species and sex-specific songs are often the subject of detailed studies regarding their evolution, responses to changing environments, involvement in social behavior, and used to design vocalization-based survey techniques to monitor population densities and trends. What is poorly understood is the value and impact of using the science and sound of gibbon vocalization and gibbon stories in education and outreach to complement nongovernmental organizations (NGOs) efforts. We present an example of how Borneo Nature Foundation, a NGOs based in Indonesia, is working to use the recordings of the songs of Bornean white-bearded gibbons (Hylobates albibarbis) to inform conservation actions and education efforts. Gibbons in Indonesia are often poorly known or understood by the public compared to orangutans (Pongo spp). We showcase how a field of study, namely primate acoustics, is an untapped resource to create digital content to engage with local, national and international communities and can be developed into educational tools in the form of storytelling, mobile apps and games, to highlight the plight of these threatened species and how to conserve them.
Saimiri cassiquiarensis cassiquiarensis (Cebidae) is a primate subspecies with a wide distribution in the Amazonian region of Brazil, Colombia, and Venezuela. However, the boundaries of its geographic range remain poorly defined. This study presents new occurrence localities for this subspecies and updates its distribution using a compiled data set of 140 occurrence records based on literature, specimens vouchered in scientific collections, and new field data to produce model-based range maps. After cleaning our data set, we updated the subspecies' extent of occurrence, which was used in model calibration. We then modeled the subspecies' range using a maximum entropy algorithm (MaxEnt). The final model was adjusted using a fixed threshold, and we revised this polygon based on known geographic barriers and parapatric congeneric ranges. Our findings indicate that this subspecies is strongly associated with lowland areas, with consistently high daily temperatures. We propose modifications to all range boundaries and estimate that 3% of the area of occupancy (AOO, as defined by IUCN) has already been lost due to deforestation, resulting in a current range of 224,469 km2. We also found that 54% of their AOO is currently covered by protected areas (PAs). Based on these results, we consider that this subspecies is currently properly classified as Least Concern, because it occupies an extensive range, which is relatively well covered by PAs, and is currently experiencing low rates of deforestation.
The consumption of primates is integral to the traditional subsistence strategies of many Indigenous communities throughout Amazonia. Understanding the overall health of primates harvested for food in the region is critical to Indigenous food security and thus, these communities are highly invested in long-term primate population health. Here, we describe the establishment of a surveillance comanagement program among the Waiwai, an Indigenous community in the Konashen Amerindian Protected Area (KAPA). To assess primate health in the KAPA, hunters performed field necropsies on primates harvested for food and tissues collected from these individuals were analyzed using histopathology. From 2015 to 2019, hunters conducted 127 necropsies across seven species of primates. Of this sample, 82 primates (between 2015 and 2017) were submitted for histopathological screening. Our histopathology data revealed that KAPA primates had little evidence of underlying disease. Of the tissue abnormalities observed, the majority were either due to diet (e.g., hepatocellular pigment), degenerative changes resulting from aging (e.g., interstitial nephritis, myocyte lipofusion), or nonspecific responses to antigenic stimulation (renal and splenic lymphoid hyperplasia). In our sample, 7.32% of individuals had abnormalities that were consistent with a viral etiology, including myocarditis and hepatitis. Internal parasites were observed in 53.66% of individuals and is consistent with what would be expected from a free-ranging primate population. This study represents the importance of baseline data for long-term monitoring of primate populations hunted for food. More broadly, this research begins to close a critical gap in zoonotic disease risk related to primate harvesting in Amazonia, while also demonstrating the benefits of partnering with Indigenous hunters and leveraging hunting practices in disease surveillance and primate population health assessment.
Research on manipulative abilities in nonhuman primates, in the context of hominid evolution, has mostly focused on manual/pedal postures considered as static behaviors. While these behavioral repertoires highlighted the range of manipulative abilities in many species, manipulation is a dynamic process that mostly involves successive types of grips before reaching its goal. The present study aims to investigate the use of manual/pedal postures in zoo-housed bonobos in diverse dynamic food processing by using an innovative approach: the optimal matching analysis that compares sequences (i.e., succession of grasping postures) with each other. To characterize the manipulative techniques spontaneously employed by bonobos, we performed this sequential analysis of manual/pedal postures during 766 complete feeding sequences of 17 individuals. We analyzed the effectiveness with a score defined by a partial proxy of food intake (i.e., the number of mouthfuls) linked to a handling score measuring both the diversity and changes of manual postures during each sequence. We identified four techniques, used differently depending on the physical substrate on which the individual performed food manipulation and the food physical properties. Our results showed that manipulative techniques were more complex (i.e., higher handling score) for large foods and on substrates with lower stability. But the effectiveness score was not significantly lower for these items since manipulative complexity seemed to be compensated by a greater number of mouthfuls. It appeared that the techniques employed involved a trade-off between manipulative complexity and the amount of food ingested. This study allowed us to test and validate innovative analysis methods that are applicable to diverse ethological studies involving sequential events. Our results bring new data for a better understanding of the evolution of manual abilities in primates in association with different ecological contexts and both terrestrial and arboreal substrates and suggest that social and individual influences need to be explored further.
Edge effects result from the penetration to varying depths and intensities, of abiotic and biotic conditions from the surrounding non-forest matrix into the forest interior. Although 70% of the world's forests are within 1 km of a forest edge, making edge effects a dominant feature of most forest habitats, there are few empirical data on inter-site differences in edge responses in primates. We used spatially explicit capture-recapture (SECR) models to determine spatial patterns of density for two species of mouse lemurs (Microcebus murinus and Microcebus ravelobensis) in two forest landscapes in northwestern Madagascar. The goal of our study was to determine if mouse lemurs displayed spatially variable responses to edge effects. We trapped animals using Sherman live traps in the Mariarano Classified Forest (MCF) and in the Ambanjabe Forest Fragment Site (AFFS) site within Ankarafantsika National Park. We trapped 126 M. murinus and 79 M. ravelobensis at MCF and 78 M. murinus and 308 M. ravelobensis at AFFS. For M. murinus, our top model predicted a positive edge response, where density increased towards edge habitats. In M. ravelobensis, our top model predicted a negative edge response, where density was lower near the forest edges and increased towards the forest interior. At regional and landscape-specific scales, SECR models estimated different density patterns between M. murinus and M. ravelobensis as a result of variation in edge distance. The spatial variability of our results using SECR models indicate the importance of studying the population ecology of primates at varying scales that are appropriate to the processes of interest. Our results lend further support to the theory that some lemurs exhibit a form of ecological flexibility in their responses to forest loss, forest fragmentation, and associated edge effects.