Cross-species pathogen spillover across ecosystem boundaries: mechanisms and theory

Abstract

Pathogen spillover between different host species is the trigger for many infectious disease outbreaks and emergence events, and ecosystem boundary areas have been suggested as spatial hotspots of spillover. This hypothesis is largely based on suspected higher rates of zoonotic disease spillover and emergence in fragmented landscapes and other areas where humans live in close vicinity to wildlife. For example, Ebola virus outbreaks have been linked to contacts between humans and infected wildlife at the rural-forest border, and spillover of yellow fever via mosquito vectors happens at the interface between forest and human settlements. Because spillover involves complex interactions between multiple species and is difficult to observe directly, empirical studies are scarce, particularly those that quantify underlying mechanisms. In this review, we identify and explore potential ecological mechanisms affecting spillover of pathogens (and parasites in general) at ecosystem boundaries. We borrow the concept of 'permeability' from animal movement ecology as a measure of the likelihood that hosts and parasites are present in an ecosystem boundary region. We then discuss how different mechanisms operating at the levels of organisms and ecosystems might affect permeability and spillover. This review is a step towards developing a general theory of cross-species parasite spillover across ecosystem boundaries with the eventual aim of improving predictions of spillover risk in heterogeneous landscapes. This article is part of the theme issue 'Dynamic and integrative approaches to understanding pathogen spillover'.

Keywords: cross-boundary spillover; disease ecology; edge effects; emerging infectious disease; fragmentation; spillover theory.

Figure 1.

Conceptual model of how host and parasite characteristics affect boundary permeability to spillover. Non-exhaustive list of different ways in which general ecological mechanisms can affect parasite spillover across ecosystem boundaries. Purple and yellow background colours represent adjacent ecosystems, and the region of overlap represents their boundary. Red lines illustrate spillover rate at the different locations (ecosystem interiors and boundary). Grey boxes indicate the spatial extent of source, bridge/vector, and recipient hosts, as well as the parasite. (Online version in colour.)

Figure 2.

For a given ecosystem patch area, a higher perimeter-to-area-ratio corresponds with increased boundary length. This corresponds with increased potential for spillover across ecosystem boundaries. (Online version in colour.)