Abstract
Invasive soilborne plant pathogens cause substantial damage to crops and natural populations, but our understanding of how to prevent their epidemics or reduce their damage is limited. A key and experimentally-tested concept in the epidemiology of soilborne plant diseases is that of a threshold spacing between hosts below which epidemics (invasive spread) can occur. We extend this paradigm by examining how plant-root growth may alter the conditions for occurrence of soilborne pathogen epidemics in plant populations. We hypothesise that host-root growth can 1) increase the probability of pathogen transmission between neighbouring plants and, consequently, 2) decrease the threshold spacing for epidemics to occur. We predict that, in systems initially below their threshold conditions, root growth can trigger soilborne pathogen epidemics through a switch from non-invasive to invasive behaviour, while in systems above threshold conditions root growth can enhance epidemic development. As an example pathosystem, we studied the fungus Rhizoctonia solani on sugar beet in field experiments. To address hypothesis 1, we recorded infections within inoculum-donor and host-recipient pairs of plants with differing spacing. We translated these observations into the individual-level concept of pathozone, a host-centred form of dispersal kernel. To test hypothesis 2 and our prediction, we used the pathozone to parameterise a stochastic model of pathogen spread in a host population, contrasting scenarios of spread with and without host growth. Our results support our hypotheses and prediction. We suggest that practitioners of agriculture and arboriculture account for root system expansion in order to reduce the risk of soilborne-disease epidemics. We discuss changes in crop design, including increasing plant spacing and using crop mixtures, for boosting crop resilience to invasion and damage by soilborne pathogens. We speculate that the disease-induced root growth observed in some pathosystems could be a pathogen strategy to increase its population through host manipulation.
Highlights
Invasions by plant pathogens can significantly impact plant communities [1,2,3] and cause substantial economic losses in agricultural and silvicultural systems [4,5]
Mathematical models allow the prediction of threshold conditions for pathogen invasion in host populations [8,9,10] on which some criteria for optimal disease control are based [6,11]
For most soilborne plant diseases, pathogen spread occurs predominantly between plants that have grown as close neighbours [7,12,13,14], posing stricter threshold conditions for pathogen invasion than in well mixed populations, e.g., a higher transmission rate [12,15]
Summary
Invasions by plant pathogens can significantly impact plant communities [1,2,3] and cause substantial economic losses in agricultural and silvicultural systems [4,5]. For most soilborne plant diseases, pathogen spread occurs predominantly between plants that have grown as close neighbours [7,12,13,14], posing stricter threshold conditions for pathogen invasion than in well mixed populations, e.g., a higher transmission rate [12,15]. In these systems, there is a close association with the concept of percolation threshold [16], i.e., a critical probability of connection (and transmission, in our case) between neighbour sites in a lattice. We investigate experimentally and theoretically, how host growth can alter epidemic thresholds (invasive spread) for soilborne plant pathogens
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