Top-down and bottom-up controls on plant pathogens: Viral prevalence in grasslands

Most pathogens exist within complicated food webs of hosts and their resources, competitors, and consumers.  While direct pathogen-host interactions are often well-described, infection rates also may be indirectly determined by the host’s consumers and competitors or supply of the host’s resources.  Here we examine the indirect role of resource availability and consumers in determining the prevalence of a generalist pathogen of grasses, barley yellow dwarf virus (BYDV). Nutrients and host context have been shown to alter infection rates by this pathogen.  Recent work suggests that infection can reduce competitive ability and survivorship whereas clipping (simulated grazing) can increase survivorship in some infected hosts.  These results raise the interesting issue of the role of indirect interactions in controlling pathogen prevalence.  In particular, is infection prevalence more strongly associated with grazing (top-down) or nutrient availability (bottom-up)?  We compared BYDV infection prevalence in Bromus hordeaceus in 18 paired plots across three sites in central California with fences manipulating grazing by deer, sheep, and/or cattle.  This annual grass host was present at all sites and provided a consistent comparison of within-year infection patterns.  Soil collections provided information on site-scale resources.  Infection prevalence was substantially higher in grazed areas, but was not affected by soil chemistry or characteristics of the host community.  Thus, BYDV prevalence is indirectly controlled by top-down grazing pressure.  More generally, this result demonstrates that predicting infection rates in natural populations is not simply a function of host-pathogen interactions, but requires a more holistic approach including indirect interactions within a whole-community context.