Saturation Excess Overland Flow Accelerates the Spread of a Generalist Soil-Borne Pathogen

Plant pathogens are a major agent of disturbance in ecosystems worldwide. Disturbance by diseases which inhibit plant water uptake can alter the hydrological function of affected ecosystems. However, many plant pathogens are also sensitive to soil moisture and can be propagated by the transport of infectious tissue or reproductive structures in surface flow, so that hydrological processes can drive pathogen infection. These feed-forward and feed-back processes set up the possibility of complex ecohydrological dynamics relating plant disease and the water cycle. Here the generalist root pathogen Phytophthora cinnamomi (Pc) is used as a case study to examine the potential importance of hydrological dynamics on disease spread. A numerical model of Pc growth and dispersal is used to investigate the importance of Pc transport in intermittent surface runoff compared to more continuous rhizosphere Pc spread via diffusion-like hyphal growth. We apply and test this model at two well-studied sites of Pc infection with contrasting hydrology: a Banksia woodland in Western Australia where deep sandy soils inhibit surface runoff, and an Erica heathland in the Spanish Central Plateau where relatively shallow soils on steep slopes generate intermittent saturation excess overland flow. Predictions of Pc spatial spread at the Spanish site improve when Pc transport in runoff is incorporated into the model, while no such improvements arise at the Australian site. Omitting transport in overland flow from model predictions at the Spanish site results in an average under-prediction of final pathogen patch areas by 350 m2 for each year of growth between observations, highlighting the importance of surface hydrological transport to Pc growth and spread and need for further studies. Hydrological theories that predict the occurrence of overland flow based on soil, topographic, and climate properties can be used to better incorporate this transport pathway and the influence of local hydrological processes in existing Pc risk assessment methods.