The ecology of enteric bacterial transmission among apes, humans, and livestock in Bwindi Impenetrable and Kibale National Parks, Uganda

Abstract

The problem of disease transmission between apes and humans has been a subject of great concern, but few studies have examined this from an ecological perspective, or confirmed transmission using genetic methods. The main goal of this thesis was to understand how and why ape anthroponoses and zoonoses emerge in tropical forest ecosystems and to suggest control measures that can be put into place to stop the spread of such infections. In order to achieve this, one hundred and forty households in the study area in and around Bwindi Impenetrable and Kibale National Parks were surveyed about their demographics, health, and interaction with wild primates. At the same time fecal samples were collected from humans, domestic animals and apes to isolate Escherichia coli, a common bacterium, which were then genotyped using a “DNA fingerprinting” method. Data were used to examine whether habitat overlap influences rates and patterns of bacterial transmission among humans, domestic animals and apes. Findings indicate that gorilla populations that frequently interact with people and domestic animals harbor E. coli bacteria that are genetically similar to those from the people or domestic animals with which they interact. On the other hand, gorilla populations with limited interaction with humans harbor E. coli bacteria more genetically distant from those of local people. Additionally, antibiotic resistance was high in bacteria from humans, lower in bacteria from domestic animals, and lowest in bacteria from mountain gorillas; within gorillas, groups with no or little overlap with humans harbored bacteria with the lowest levels of resistance. Genetic distances between human and livestock bacteria were generally very low, indicating high rates of bacterial gene flow between humans and their domestic animals. Data showed that people who did not regularly wash their hands before eating harbored bacteria approximately twice as similar genetically to bacteria of their livestock as did people who regularly washed their hands before eating. Furthermore, findings indicate that crop raiding is contributing to pathogen transmission between apes and humans and domestic livestock in Bwindi. People and livestock from Bwindi tended to harbor E. coli bacteria more similar to those of crop-raiding gorillas with “high overlap” than to bacteria from “low overlap” gorillas that do not raid crops. This pattern was, however, different for Kibale, where humans and their livestock living near Kibale harbored bacteria that were genetically similar to those from chimpanzees at a remote location and with “low overlap,” but less similar to bacteria from local “high overlap” chimpanzees. The reasons for this paradoxical result in Kibale are unclear, but may have to do with patterns of water flow. Although almost all animals in the two locations contributed to crop raiding, the role of this practice in pathogen transmission was only examined in apes. In both Bwindi and Kibale, primates (most often baboons) were responsible for the majority of crop raiding events, followed by bush pigs. Apes (chimpanzees and mountain gorillas) were not highly implicated in the crop raiding events, with apes mainly targeting banana plantations. Patterns of genetic similarity and antibiotic resistance among E. coli from populations of apes, humans, and livestock indicate that habitat overlap between species affects the dynamics of gastrointestinal bacterial transmission, perhaps through domestic animal intermediates and the physical environment; and that patterns of human hygiene affect human-livestock bacterial transmission in rural settings. Limiting transmission would benefit human and domestic animal health and ape conservation. These results highlight not only the potential importance of crop-raiding as a factor increasing infectious disease transmission risk between apes and people in areas of human-ape conflict, but also the variability of this trend among locations.