Selective deforestation and exposure of African wildlife to bat-borne viruses

Proposed mechanisms of zoonotic virus spillover often posit that wildlife transmission and amplification precede human outbreaks. Between 2006 and 2012, the palm Raphia farinifera, a rich source of dietary minerals for wildlife, was nearly extirpated from Budongo Forest, Uganda. Since then, chimpanzees, black-and-white colobus, and red duiker were observed feeding on bat guano, a behavior not previously observed. Here we show that guano consumption may be a response to dietary mineral scarcity and may expose wildlife to bat-borne viruses. Videos from 2017–2019 recorded 839 instances of guano consumption by the aforementioned species. Nutritional analysis of the guano revealed high concentrations of sodium, potassium, magnesium and phosphorus. Metagenomic analyses of the guano identified 27 eukaryotic viruses, including a novel betacoronavirus. Our findings illustrate how “upstream” drivers such as socioeconomics and resource extraction can initiate elaborate chains of causation, ultimately increasing virus spillover risk.

Spillover of viruses from wildlife to humans is often thought to be preceded by viral transmission and amplification among wildlife. For example, human ebolavirus outbreaks in Africa follow sylvatic transmission cycles in non-human primates and ungulates, with humans likely becoming infected through contact with carcasses^1,2,3. Similarly, epidemiological data and analyses of inferred viral genomic recombination suggest that approximately half of human-infecting coronaviruses underwent transmission from wildlife reservoirs to humans through intermediary hosts^4,5. Despite the high social and economic costs of zoonoses⁶, the mechanisms underlying such antecedent virus transmission within animals remain poorly understood.

Budongo Forest Reserve, western Uganda, contains approximately 482 km² of medium-altitude, semi-deciduous forest⁷ and is located in the Albertine Rift, a region of exceptional biodiversity and endemism⁸. Until approximately 2008, the swamp forests of Budongo contained Raphia farinifera, a palm that, when decaying, provided a high-quality source of essential dietary minerals to wildlife⁹. Between 2006 and 2012, tobacco farming increased markedly in the area due to rising international demand and incentives from tobacco companies with longstanding operations in Uganda¹⁰. As a result, local farmers nearly extirpated R. farinifera because of its usefulness for making strings on which to dry tobacco leaves^9,11. Budongo’s eastern chimpanzees (Pan troglodytes schweinfurthii) altered their feeding behavior in response to this loss of a primary source of dietary minerals, increasingly consuming alternative sources such as clay, termite mounds, and the decaying pith of other tree species⁹. In 2017, we observed a never-before documented behavior by several species of wildlife in Budongo, including chimpanzees: the consumption of bat guano.

Here we present the results of an investigation as to whether this behavior could be an adaptation to dietary mineral scarcity, analogous to what has been documented for similar behaviors at this site⁹. We also investigate whether guano consumption could be an ecological mechanism whereby wildlife such as chimpanzees might be exposed to bat-borne viruses. We document high frequencies of guano consumption by three species of wildlife in Budongo, high concentrations of essential dietary minerals in the guano, and diverse bat-borne viruses in the guano, including a novel betacoronavirus within the Hibecovirus subgenus. These results illustrate how remote upstream forces can induce unanticipated causal chains that alter wildlife ecology and behavior, one result of which may be to increase virus spillover risk.