Community health and human-animal contacts on the edges of Bwindi Impenetrable National Park, Uganda

Cross-species transmission of pathogens is intimately linked to human and environmental health. With limited healthcare and challenging living conditions, people living in poverty may be particularly susceptible to endemic and emerging diseases. Similarly, wildlife is impacted by human influences, including pathogen sharing, especially for species in close contact with people and domesticated animals. Here we investigate human and animal contacts and human health in a community living around the Bwindi Impenetrable National Park (BINP), Uganda. We used contact and health survey data to identify opportunities for cross-species pathogen transmission, focusing mostly on people and the endangered mountain gorilla. We conducted a survey with background questions and self-reported diaries to investigate 100 participants' health, such as symptoms and behaviours, and contact patterns, including direct contacts and sightings over a week. Contacts were revealed through networks, including humans, domestic, peri-domestic, and wild animals for 1) network of contacts seen in the week of background questionnaire completion, 2) network of contacts seen during the diary week. Participants frequently felt unwell during the study, reporting from one to 10 disease symptoms at different intensity levels (maximum of seven symptoms in one day), with severe symptoms comprising 6.4% of the diary records and tiredness and headaches the most common symptoms. Besides human-human contacts, direct contacts with livestock and peri-domestic animals were the most common. Wildlife contacts were the rarest, including one direct contact with gorilla with a concerning timeline of reported symptoms. The contact networks were moderately connected and revealing a preference in contacts within the same species or taxon and within their groups. Despite sightings of wildlife being much more common than touching, one participant declared direct contact with a mountain gorilla during the week. Gorillas were seen very close to six animal taxa (including themselves) considering all interaction types, mostly seen closer to other gorillas, but also people and domestic animals. Our findings reveal a local human population with recurrent symptoms of illness in a location with intense exposure to factors that can increase pathogen transmission, such as direct contact with domestic and wild animals and proximity among animal species. Despite significant biases and study limitations, the information generated here can guide future studies, such as models for disease spread and One Health interventions.

Heterogeneity in patterns of helminth infections across populations of mountain gorillas (Gorilla beringei beringei)

Conservation efforts have led to the recovery of the endangered mountain gorilla populations. Due to their limited potential for spatial expansion, population densities increased, which may alter the epidemiology of infectious diseases. Recently, clinical gastrointestinal illnesses linked to helminth infections have been recorded in both gorilla populations. To understand drivers and patterns of helminth infections we quantified strongylid and tapeworm infections across both Virunga Massif and Bwindi populations using fecal egg counts. We assessed the impact of age, sex, group size, season and spatial differences used as a proxy, which reflects observed variation in the occurrence of gastrointestinal problems, vegetation types, gorilla subpopulation growth and associated social structure on helminth infections. We revealed striking geographic differences in strongylid infections with higher egg counts mostly in areas with high occurrences of gastrointestinal disease. Increased helminth egg counts were also associated with decreasing group size in some areas. Observed spatial differences may reflect mutual effects of variations in subpopulation growth rates, gorilla social structure, and vegetation associated with altitude across mountain gorilla habitat. Helminth infection intensities in Virunga gorillas were lowest in the youngest and the oldest animals. Elucidating parasite infection patterns of endangered species with low genetic diversity is crucial for their conservation management.

Development of 79 SNP markers to individually genotype and sex-type endangered mountain gorillas (Gorilla beringei beringei)

The mountain gorilla (Gorilla beringei beringei) is one of two endangered subspecies of eastern gorilla. The principle approach to monitoring the two extant mountain gorilla populations has been to use fecal surveys to obtain DNA profiles for individuals that are then used for capture-recapture-based estimates of abundance. To date, 11 to 14 microsatellites have been used for this purpose. To adapt to ongoing changes in genotyping technologies and to facilitate the analysis of fecal DNA samples by multiple laboratories, we developed a panel of single nucleotide polymorphism (SNP) markers that can be used for future gorilla monitoring. We used published short read data sets for 3 individuals to develop a suite of 79 SNPs, including two sex markers, for a Fluidigm platform. This marker set provided high resolution to differentiate individuals and will facilitate future monitoring, leaving room for additional SNPs to be included in a 96-assay format.

Human Respiratory Syncytial Virus Detected in Mountain Gorilla Respiratory Outbreaks

Respiratory illness (RI) accounts for a large proportion of mortalities in mountain gorillas (Gorilla beringei beringei), and fatal outbreaks, including disease caused by human metapneumovirus (HMPV) infections, have heightened concern about the risk of human pathogen transmission to this endangered species, which is not only critically important to the biodiversity of its ecosystem but also to the economies of the surrounding human communities. Our goal was to conduct a molecular epidemiologic study to detect the presence of HRSV and HMPV in fecal samples from wild human-habituated free-ranging mountain gorillas in Rwanda and to evaluate the role of these viruses in RI outbreaks. Fecal samples were collected from gorillas with clinical signs of RI between June 2012 and February 2013 and tested by real-time and conventional polymerase chain reaction (PCR) assays; comparison fecal samples were obtained from gorillas without clinical signs of RI sampled during the 2010 Virunga gorilla population census. PCR assays detected HMPV and HRSV first in spiked samples; subsequently, HRSV-A, the worldwide-circulating ON1 genotype, was detected in 12 of 20 mountain gorilla fecal samples collected from gorillas with RI during outbreaks, but not in samples from animals without respiratory illness. Our findings confirmed that pathogenic human respiratory viruses are transmitted to gorillas and that they are repeatedly introduced into mountain gorilla populations from people, attesting to the need for stringent biosecurity measures for the protection of gorilla health.

Violent encounters between social units hinder the growth of a high-density mountain gorilla population

Density-dependent processes such as competition for resources, migration, predation, and disease outbreaks limit the growth of natural populations. The analysis of 50 years of mountain gorilla data reveals that social behavior changes observed at high group density may also affect population growth in social species. A sudden increase in social group density observed in 2007 caused a threefold increase in the rate of violent encounters between social units (groups and solitary males). A fivefold increase in the rate of infanticide and seven cases of lethal fights among mature males were subsequently recorded, and the annual subpopulation growth rate declined by half between 2000 and 2017. The increase in infanticide alone explains 57% of this decline. These findings highlight the complex relationship between population density and growth in social species and hold important implications for the management of island populations.

Comparing measures of social complexity: larger mountain gorilla groups do not have a greater diversity of relationships

Social complexity reflects the intricate patterns of social interactions in societies. Understanding social complexity is fundamental for studying the evolution of diverse social systems and the cognitive innovations used to cope with the demands of social life. Social complexity has been predominantly quantified by social unit size, but newer measures of social complexity reflect the diversity of relationships. However, the association between these two sets of measures remains unclear. We used 12 years of data on 13 gorilla groups to investigate how measures of social complexity relate to each other. We found that group size was a poor proxy for relationship diversity and that the social complexity individuals experienced within the same group varied greatly. Our findings demonstrate two fundamental takeaways: first, that the number of relationships and the diversity of those relationships represent separate components of social complexity, both of which should be accounted for; and second, that social complexity measured at the group level may not represent the social complexity experienced by individuals in those groups. These findings suggest that comprehensive studies of social complexity, particularly those relating to the social demands faced by individuals, may require fine-scale social data to allow accurate comparisons across populations and species.