Endangered mountain gorillas and COVID-19: One health lessons for prevention and preparedness during a global pandemic.

The world's 1063 mountain gorillas (Gorilla beringei beringei) live in two subpopulations at the borders of the Democratic Republic of Congo, Rwanda, and Uganda. The majority of mountain gorillas are human-habituated to facilitate tourism and research, which brings mountain gorillas into close proximity of people daily. Wild great apes are proven to be susceptible to human pathogens, including viruses that have caused fatal respiratory disease in mountain gorillas (e.g., human metapneumovirus1 ). This is the result of the close genetic relatedness of humans and gorillas as species, and the structural and genetic similarity in molecular receptors that allow viruses to infect cells2 . At the time of writing, there is no evidence that severe acute respiratory syndrome coronavirus 2, the coronavirus that causes coronavirus disease 19 (COVID-19), has infected a mountain gorilla. However, due to the significant potential for human-to-gorilla transmission, mountain gorilla range States took immediate steps to minimize the COVID-19 threat. These actions included a combination of preventive practice around gorillas and other great apes (e.g., mandatory face mask use, increased "social" minimum distancing from gorillas) as well as human public health measures (e.g., daily health/fever screenings, COVID-19 screening, and quarantines). Minimization of the COVID-19 threat also required socioeconomic decision-making and political will, as all gorilla tourism was suspended by late March 2020 and guidelines developed for tourism reopening. A consortium that collaborates and coordinates on mountain gorilla management and conservation, working within an intergovernmental institutional framework, took a multifaceted One Health approach to address the COVID-19 threat to mountain gorillas by developing a phased contingency plan for prevention and response. The aim of this paper is to describe how range States and partners achieved this collaborative planning effort, with intent that this real-world experience will inform similar actions at other great ape sites.

Agricultural expansion as risk to endangered wildlife: Pesticide exposure in wild chimpanzees and baboons displaying facial dysplasia.

Prenatal exposure to environmental endocrine disruptors can affect development and induce irreversible abnormalities in both humans and wildlife. The northern part of Kibale National Park, a mid-altitude rainforest in western Uganda, is largely surrounded by industrial tea plantations and wildlife using this area (Sebitoli) must cope with proximity to human populations and their activities. The chimpanzees and baboons in this area raid crops (primarily maize) in neighboring gardens. Sixteen young individuals of the 66 chimpanzees monitored (25%) exhibit abnormalities including reduced nostrils, cleft lip, limb deformities, reproductive problems and hypopigmentation. Each pathology could have a congenital component, potentially exacerbated by environmental factors. In addition, at least six of 35 photographed baboons from a Sebitoli troop (17%) have similar severe nasal deformities. Our inquiries in villages and tea factories near Sebitoli revealed use of eight pesticides (glyphosate, cypermethrin, profenofos, mancozeb, metalaxyl, dimethoate, chlorpyrifos and 2,4-D amine). Chemical analysis of samples collected from 2014 to 2016 showed that mean levels of pesticides in fresh maize stems and seeds, soils, and river sediments in the vicinity of the chimpanzee territory exceed recommended limits. Notably, excess levels were found for total DDT and its metabolite pp'-DDE and for chlorpyrifos in fresh maize seeds and in fish from Sebitoli. Imidacloprid was detected in coated maize seeds planted at the edge the forest and in fish samples from the Sebitoli area, while no pesticides were detected in fish from central park areas. Since some of these pesticides are thyroid hormone disruptors, we postulate that excessive pesticide use in the Sebitoli area may contribute to facial dysplasia in chimpanzees and baboons through this endocrine pathway. Chimpanzees are considered as endangered by IUCN and besides their intrinsic value and status as closely related to humans, they have major economic value in Uganda via ecotourism. Identifying and limiting potential threats to their survival such be a conservation priority.

Nodular Worm Infections in Wild Non-human Primates and Humans Living in the Sebitoli Area (Kibale National Park, Uganda): Do High Spatial Proximity Favor Zoonotic Transmission?

BACKGROUND: Nodular Oesophagostomum genus nematodes are a major public health concern in some African regions because they can be lethal to humans. Their relatively high prevalence in people has been described in Uganda recently. While non-human primates also harbor Oesophagostomum spp., the epidemiology of this oesophagostomosis and the role of these animals as reservoirs of the infection in Eastern Africa are not yet well documented. METHODOLOGY/PRINCIPAL FINDINGS: The present study aimed to investigate Oesophagostomum infection in terms of parasite species diversity, prevalence and load in three non-human primates (Pan troglodytes, Papio anubis, Colobus guereza) and humans living in close proximity in a forested area of Sebitoli, Kibale National Park (KNP), Uganda. The molecular phylogenetic analyses provided the first evidence that humans living in the Sebitoli area harbored O. stephanostomum, a common species in free-ranging chimpanzees. Chimpanzees were also infected by O. bifurcum, a common species described in human populations throughout Africa. The recently described Oesophagostomum sp. found in colobine monkeys and humans and which was absent from baboons in the neighboring site of Kanyawara in KNP (10 km from Sebitoli), was only found in baboons. Microscopic analyses revealed that the infection prevalence and parasite load in chimpanzees were significantly lower in Kanyawara than in Sebitoli, an area more impacted by human activities at its borders. CONCLUSIONS/SIGNIFICANCE: Three different Oesophagostomum species circulate in humans and non-human primates in the Sebitoli area and our results confirm the presence of a new genotype of Oesophagostomum recently described in Uganda. The high spatiotemporal overlap between humans and chimpanzees in the studied area coupled with the high infection prevalence among chimpanzees represent factors that could increase the risk of transmission for O. stephanostomum between the two primate species. Finally, the importance of local-scale research for zoonosis risk management is important because environmental disturbance and species contact can differ, leading to different parasitological profiles between sites that are close together within the same forest patches.

Chimpanzees facing a dangerous situation: A high-traffic asphalted road in the Sebitoli area of Kibale National Park, Uganda.

Despite the spread of road infrastructures throughout Africa to support regional development, industry, and tourism, few studies have examined how wild animals adapt their behavior and ecology in road-forest ecotones. Indeed, while numerous studies have demonstrated chimpanzee adaptability in anthropogenic landscapes, none have examined the effects of asphalted highways on wild chimpanzee behaviors. In a 29-month survey, we assessed the dangers posed by an asphalted road crossing the Sebitoli area of Kibale National Park (Uganda). We analyzed 122 individual chimpanzee crossings. Although the asphalted road represents a substantial threat to crossing animals (89 motorized vehicles per hour use this road and individuals of six different primate species were killed in 1 year), chimpanzees took into account this risk. More than 90% of the individuals looked right and left before and while crossing. Chimpanzees crossed in small subgroups (average 2.7 subgroups of 2.1 individuals per crossing event). Whole parties crossed more rapidly when chimpanzees were more numerous in the crossing groups. The individuals most vulnerable to the dangers of road crossing (females with dependents, immature, and severely injured individuals) crossed less frequently compared with non-vulnerable individuals (lone and healthy adolescents and adults). Moreover, healthy adult males, who were the most frequent crossing individuals, led progressions more frequently when crossing the road than when climbing or descending feeding trees. Almost 20% of the individuals that crossed paid attention to conspecifics by checking on them or waiting for them while crossing. These observations are relevant for our understanding of adaptive behavior among chimpanzees in human-impacted habitats. Further investigations are needed to better evaluate the effects of busy roads on adolescent female dispersal and on their use of territories. Mitigation measures (e.g., bridges, underpasses, reduced speed limits, speed-bumps, signposts, or police controls) should be established in this area.

Two Cases of Cleft Lip and Other Congenital Anomalies in Wild Chimpanzees Living in Kibale National Park, Uganda.

DESIGN: Observations of wild chimpanzees ( Pan troglodytes schweinfurthii) were conducted in Kibale National Park, Uganda, at the sites of Sebitoli and Ngogo. RESULTS: We report the first two cases of cleft lip in wild chimpanzees. Additionally, some other chimpanzees in the Sebitoli community show facial dysplasia and congenital anomalies, such as patches of depigmented hairs and limb defects. CONCLUSIONS: Cleft lip has been documented in several species of nonhuman primates, but much remains unknown about the occurrence of cleft lip and cleft palate in great apes, probably because such malformations are rare, wild apes are difficult to monitor and observe, and severe cases associated with cleft palates render suckling impossible and lead to early death of infants. The genetic basis of such defects in great apes warrants investigation, as does the possibility that environmental toxins contribute to their etiology in Kibale in ways that could affect humans as well.

Wild chimpanzees on the edge: nocturnal activities in croplands.

In a rapidly changing landscape highly impacted by anthropogenic activities, the great apes are facing new challenges to coexist with humans. For chimpanzee communities inhabiting encroached territories, not bordered by rival conspecifics but by human agricultural fields, such boundaries are risky areas. To investigate the hypothesis that they use specific strategies for incursions out of the forest into maize fields to prevent the risk of detection by humans guarding their field, we carried out video recordings of chimpanzees at the edge of the forest bordered by a maize plantation in Kibale National Park, Uganda. Contrary to our expectations, large parties are engaged in crop-raids, including vulnerable individuals such as females with clinging infants. More surprisingly chimpanzees were crop-raiding during the night. They also stayed longer in the maize field and presented few signs of vigilance and anxiety during these nocturnal crop-raids. While nocturnal activities of chimpanzees have been reported during full moon periods, this is the first record of frequent and repeated nocturnal activities after twilight, in darkness. Habitat destruction may have promoted behavioural adjustments such as nocturnal exploitation of open croplands.

Suitable habitats for endangered frugivorous mammals: small-scale comparison, regeneration forest and chimpanzee density in Kibale National Park, Uganda.

Landscape patterns and chimpanzee (Pan troglodytes schweinfurthii) densities in Kibale National Park show important variation among communities that are geographically close to one another (from 1.5 to 5.1 chimpanzees/km2). Anthropogenic activities inside the park (past logging activities, current encroachment) and outside its limits (food and cash crops) may impact the amount and distribution of food resources for chimpanzees (frugivorous species) and their spatial distribution within the park. Spatial and temporal patterns of fruit availability were recorded over 18 months at Sebitoli (a site of intermediate chimpanzee density and higher anthropic pressure) with the aim of understanding the factors explaining chimpanzee density there, in comparison to results from two other sites, also in Kibale: Kanyawara (low chimpanzee density) and Ngogo (high density, and furthest from Sebitoli). Because of the post-logging regenerating status of the forest in Sebitoli and Kanyawara, smaller basal area (BA) of fruiting trees most widely consumed by the chimpanzees in Kanyawara and Sebitoli was expected compared to Ngogo (not logged commercially). Due to the distance between sites, spatial and temporal fruit abundance in Sebitoli was expected to be more similar to Kanyawara than to Ngogo. While species functional classes consumed by Sebitoli chimpanzees (foods eaten during periods of high or low fruit abundance) differ from the two other sites, Sebitoli is very similar to Kanyawara in terms of land-cover and consumed species. Among feeding trees, Ficus species are particularly important resources for chimpanzees at Sebitoli, where their basal area is higher than at Kanywara or Ngogo. Ficus species provided a relatively consistent supply of food for chimpanzees throughout the year, and we suggest that this could help to explain the unusually high density of chimpanzees in such a disturbed site.

Facial dysplasia in wild chimpanzees.

At least 10% of the Sebitoli chimpanzee community of the Kibale National Park (Uganda) present a characteristic facial phenotype with flattened nose, reduced nostrils, and concave mid-face. Affected individuals do not present skin lesions, and also young infants are affected. We suggest, therefore, a congenital origin of this defect.