Viruses in sanctuary chimpanzees across Africa.

Infectious disease is a major concern for both wild and captive primate populations. Primate sanctuaries in Africa provide critical protection to thousands of wild-born, orphan primates confiscated from the bushmeat and pet trades. However, uncertainty about the infectious agents these individuals potentially harbor has important implications for their individual care and long-term conservation strategies. We used metagenomic next-generation sequencing to identify viruses in blood samples from chimpanzees (Pan troglodytes) in three sanctuaries in West, Central, and East Africa. Our goal was to evaluate whether viruses of human origin or other "atypical" or unknown viruses might infect these chimpanzees. We identified viruses from eight families: Anelloviridae, Flaviviridae, Genomoviridae, Hepadnaviridae, Parvoviridae, Picobirnaviridae, Picornaviridae, and Rhabdoviridae. The majority (15/26) of viruses identified were members of the family Anelloviridae and represent the genera Alphatorquevirus (torque teno viruses) and Betatorquevirus (torque teno mini viruses), which are common in chimpanzees and apathogenic. Of the remaining 11 viruses, 9 were typical constituents of the chimpanzee virome that have been identified in previous studies and are also thought to be apathogenic. One virus, a novel tibrovirus (Rhabdoviridae: Tibrovirus) is related to Bas-Congo virus, which was originally thought to be a human pathogen but is currently thought to be apathogenic, incidental, and vector-borne. The only virus associated with disease was rhinovirus C (Picornaviridae: Enterovirus) infecting one chimpanzee subsequent to an outbreak of respiratory illness at that sanctuary. Our results suggest that the blood-borne virome of African sanctuary chimpanzees does not differ appreciably from that of their wild counterparts, and that persistent infection with exogenous viruses may be less common than often assumed.

Observational approaches to chimpanzee behavior in an African sanctuary: Implications for research, welfare, and capacity-building.

Research in African ape sanctuaries has emerged as an important context for our understanding of comparative cognition and behavior. While much of this work has focused on experimental studies of cognition, these animals semi-free-range in forest habitats and therefore can also provide important information about the behavior of primates in socioecologically-relevant naturalistic contexts. In this "New Approaches" article, we describe a project where we implemented a synthetic program of observational data collection at Ngamba Island Chimpanzee Sanctuary in Uganda, directly modeled after long-term data collection protocols at the Kibale Chimpanzee Project in Uganda, a wild chimpanzee field site. The foundation for this project was a strong partnership between sanctuary staff, field site staff, and external researchers. We describe how we developed a data-collection protocol through discussion and collaboration among these groups, and trained sanctuary caregivers to collect novel observational data using these protocols. We use these data as a case study to examine: (1) how behavioral observations in sanctuaries can inform primate welfare and care practices, such as by understanding aggression within the group; (2) how matched observational protocols across sites can inform our understanding of primate behavior across different contexts, including sex differences in social relationships; and (3) how more robust collaborations between foreign researchers and local partners can support capacity-building in primate range countries, along with mentoring and training students more broadly.

Effects of body region and time on hair cortisol concentrations in chimpanzees (Pan troglodytes).

Hair cortisol concentrations (HCC) are increasingly recognized as an integrated measure of the systemic cortisol secretion. Yet, we still know very little about confounding effects on HCC in animals. The present study therefore used hair from semi-wild and zoo living chimpanzees to investigate (1) intra-individual variability of HCC (body-region effect), and (2) the stability of HCC along the hair shaft (traditionally called the washout effect). Our results indicate that absolute HCC varied substantially between certain body regions, but a factor analysis revealed that these HCC differences were mainly attributable to one common source of variance. Thus, hair from all body regions provides similar biological signals and can be mixed, albeit at the cost of a lower signal-to-noise ratio. With regard to potential underlying mechanisms, we studied skin blood flow, as observed through thermal images from one chimpanzee. We found the general HCC pattern was reflected in differences in surface body temperature observed in this individual in three out of four body regions. In a separate set of samples, we found first evidence to suggest that the systematic cortisol decrease along the hair shaft, as observed in humans, is also present in chimpanzee hair. The effect was more pronounced in semi-wild than in zoo chimpanzees presumably due to more exposure to ambient weather conditions.

Viruses in saliva from sanctuary chimpanzees (Pan troglodytes) in Republic of Congo and Uganda.

Pathogen surveillance for great ape health monitoring has typically been performed on non-invasive samples, primarily feces, in wild apes and blood in sanctuary-housed apes. However, many important primate pathogens, including known zoonoses, are shed in saliva and transmitted via oral fluids. Using metagenomic methods, we identified viruses in saliva samples from 46 wild-born, sanctuary-housed chimpanzees at two African sanctuaries in Republic of Congo and Uganda. In total, we identified 20 viruses. All but one, an unclassified CRESS DNA virus, are classified in five families: Circoviridae, Herpesviridae, Papillomaviridae, Picobirnaviridae, and Retroviridae. Overall, viral prevalence ranged from 4.2% to 87.5%. Many of these viruses are ubiquitous in primates and known to replicate in the oral cavity (simian foamy viruses, Retroviridae; a cytomegalovirus and lymphocryptovirus; Herpesviridae; and alpha and gamma papillomaviruses, Papillomaviridae). None of the viruses identified have been shown to cause disease in chimpanzees or, to our knowledge, in humans. These data suggest that the risk of zoonotic viral disease from chimpanzee oral fluids in sanctuaries may be lower than commonly assumed.

Large Comparative Analyses of Primate Body Site Microbiomes Indicate that the Oral Microbiome Is Unique among All Body Sites and Conserved among Nonhuman Primates.

The study of the mammalian microbiome serves as a critical tool for understanding host-microbial diversity and coevolution and the impact of bacterial communities on host health. While studies of specific microbial systems (e.g., in the human gut) have rapidly increased, large knowledge gaps remain, hindering our understanding of the determinants and levels of variation in microbiomes across multiple body sites and host species. Here, we compare microbiome community compositions from eight distinct body sites among 17 phylogenetically diverse species of nonhuman primates (NHPs), representing the largest comparative study of microbial diversity across primate host species and body sites. Analysis of 898 samples predominantly acquired in the wild demonstrated that oral microbiomes were unique in their clustering, with distinctive divergence from all other body site microbiomes. In contrast, all other body site microbiomes clustered principally by host species and differentiated by body site within host species. These results highlight two key findings: (i) the oral microbiome is unique compared to all other body site microbiomes and conserved among diverse nonhuman primates, despite their considerable dietary and phylogenetic differences, and (ii) assessments of the determinants of host-microbial diversity are relative to the level of the comparison (i.e., intra-/inter-body site, -host species, and -individual), emphasizing the need for broader comparative microbial analyses across diverse hosts to further elucidate host-microbial dynamics, evolutionary and biological patterns of variation, and implications for human-microbial coevolution. IMPORTANCE The microbiome is critical to host health and disease, but much remains unknown about the determinants, levels, and evolution of host-microbial diversity. The relationship between hosts and their associated microbes is complex. Most studies to date have focused on the gut microbiome; however, large gaps remain in our understanding of host-microbial diversity, coevolution, and levels of variation in microbiomes across multiple body sites and host species. To better understand the patterns of variation and evolutionary context of host-microbial communities, we conducted one of the largest comparative studies to date, which indicated that the oral microbiome was distinct from the microbiomes of all other body sites and convergent across host species, suggesting conserved niche specialization within the Primates order. We also show the importance of host species differences in shaping the microbiome within specific body sites. This large, comparative study contributes valuable information on key patterns of variation among hosts and body sites, with implications for understanding host-microbial dynamics and human-microbial coevolution.

Healthy cardiovascular biomarkers across the lifespan in wild-born chimpanzees (Pan troglodytes).

Chimpanzees (Pan troglodytes) are a crucial model for understanding the evolution of human health and longevity. Cardiovascular disease is a major source of mortality during ageing in humans and therefore a key issue for comparative research. Current data indicate that compared to humans, chimpanzees have proatherogenic blood lipid profiles, an important risk factor for cardiovascular disease in humans. However, most work to date on chimpanzee lipids come from laboratory-living populations where lifestyles diverge from a wild context. Here, we examined cardiovascular profiles in chimpanzees living in African sanctuaries, who range semi-free in large forested enclosures, consume a naturalistic diet, and generally experience conditions more similar to a wild chimpanzee lifestyle. We measured blood lipids, body weight and body fat in 75 sanctuary chimpanzees and compared them to publicly available data from laboratory-living chimpanzees from the Primate Aging Database. We found that semi-free-ranging chimpanzees exhibited lower body weight and lower levels of lipids that are risk factors for human cardiovascular disease, and that some of these disparities increased with age. Our findings support the hypothesis that lifestyle can shape health indices in chimpanzees, similar to effects observed across human populations, and contribute to an emerging understanding of human cardiovascular health in an evolutionary context. This article is part of the theme issue 'Evolution of the primate ageing process'.