Deforestation-driven food-web collapse linked to emerging tropical infectious disease, Mycobacterium ulcerans

Abstract

Generalist microorganisms are the agents of many emerging infectious diseases (EIDs), but their natural life cycles are difficult to predict due to the multiplicity of potential hosts and environmental reservoirs. Among 250 known human EIDs, many have been traced to tropical rain forests and specifically freshwater aquatic systems, which act as an interface between microbe-rich sediments or substrates and terrestrial habitats. Along with the rapid urbanization of developing countries, population encroachment, deforestation, and land-use modifications are expected to increase the risk of EID outbreaks. We show that the freshwater food-web collapse driven by land-use change has a nonlinear effect on the abundance of preferential hosts of a generalist bacterial pathogen, Mycobacterium ulcerans. This leads to an increase of the pathogen within systems at certain levels of environmental disturbance. The complex link between aquatic, terrestrial, and EID processes highlights the potential importance of species community composition and structure and species life history traits in disease risk estimation and mapping. Mechanisms such as the one shown here are also central in predicting how human-induced environmental change, for example, deforestation and changes in land use, may drive emergence.

Keywords: Buruli ulcer; French Guiana; Land-use; anthropogenic change; deforestation; emerging infectious disease; foodwebs; stable isotopes.

Fig. 1. The average δ¹⁵N and a low δ¹³C in biplot space for all recorded host and nonhost organisms from the 17 sites.

δ¹⁵N and δ¹³C were derived for each host taxon using data from the three sites analyzed for stable isotopic readings and extrapolated to the additional 14 sites. For each point, the square root–transformed mean number of M. ulcerans of the host is represented by the size of the circle.

Fig. 2. Figure showing the relationships between land-use, deforestation and M. ulcerans.

(A) Plot showing the relationship between local site niche widths and the level of agricultural and urban landscape and deforestation in a 1-km buffer zone. The change in niche width caused by deforestation appears to be a steady decline, whereas the presence of agricultural land causes a sharp drop from where there is no agriculture, before exhibiting a similar steady decline in niche width as with deforestation, albeit less extreme. (B) Plot showing decline in vulnerability and generality as niche width declines with 95% confidence intervals. (C) Plot showing metrics of the food-web networks that allow taxa, which on average carry a higher M. ulcerans load to propagate. For all taxa, along the bottom axes are the mean regional food-web metrics for vulnerability and generality (that is, a measure of the food-web metrics of sites at which they are most abundant; see Materials and Methods for details), whereas the vertical axis shows the mean regional bacterial load of M. ulcerans.