Fast‐growing annual plants drive disease spillover in multi‐host communities

Abstract Emerging infectious plant diseases threaten natural, agricultural and urban systems. Predicting pathogen spillover from one host species to another can reduce disease impacts, but traditional compartment models poorly explain plant disease because plants often experience localized rather than systemic disease. Thus, the amount of infection should be tracked within each host individual, rather than characterizing a host as infected or uninfected. Additionally, annual plants can grow and complete their life cycle on timescales comparable to disease progression, thereby creating potential for feedbacks between tissue growth and pathogen spread that could be important to disease spillover. We hypothesized that, for two plant species that differ in individual‐level growth rates and share a pathogen, the faster‐growing host supports higher pathogen levels that spill onto, and negatively affect, the slower‐growing host. This prediction follows classical apparent competition theory in which prey species with high intrinsic growth rates sustain greater predator abundances, which then suppress other, slower‐growing, prey in the community. We explored whether this theory applies to plants sharing pathogens by developing an intra‐annual host–pathogen model tracking size structure of, and degree of infection in, plant hosts. We asked how growth rates of annual plant species alter spillover from a reservoir host to focal host species, and disease amplification or dilution in annual plant communities. We found that faster‐growing host individuals supported the greatest pathogen loads compared with slower‐growing host individuals, yet they experienced smaller pathogen‐driven reductions in end‐of‐season biomass. Consistent with apparent competition predictions, pathogen spillover from reservoir to focal host species caused greatest declines in end‐of‐season biomass in focal individuals when the reservoir host was fast‐growing and focal host was slow‐growing. In communities with both fast and slow‐growing species, slower‐growing hosts generally diluted disease, while faster hosts amplified it. Synthesis . The model predicts that faster‐growing hosts are likely to be high impact reservoirs for spillover and could amplify disease in multi‐host communities. Slower‐growing hosts are likely to bear the greater impact of pathogen spillover via reduced end‐of‐season biomass. Thus, plant growth rates could be an important factor in driving outcomes of infectious disease spillover in multi‐host annual plant communities.