Source or sink: The role of plant litter as an environmental reservoir for plant pathogens

Emerging infectious plant disease is a growing threat to biodiversity and food security. Plant debris (‘litter’), a ubiquitous feature of plant communities, promotes pathogen spread in some empirical systems while hindering it in others.

To contextualize this opposing evidence, we develop two mathematical models, a plant‐litter model (plant host, litter and pathogens interact) and a plant‐only model describing obligate biotrophy. We use these models to quantify pathogen spread (i.e. pathogen reproductive number ) and the potential to colonize a new host (as measured by steady‐state pathogen density: colonization success generally requires many invasion attempts, which is facilitated by high pathogen levels). We also explore how different plant‐litter‐pathogen system configurations might evolve.

Compared to the plant‐only model, the plant‐litter model adds two new ‘production’ pathways for pathogen reproduction, and one new avenue for pathogen propagule loss. When litter acts as a source, the range of parameter space permitting pathogen establishment and spread increases. This occurs when pathogen density contributions by the two new production pathways outweigh declines by the new loss pathway. The opposite occurs when loss of pathogens via the new loss pathway outweighs the gain via the two production pathways, resulting in litter acting as a pathogen sink.

Fitness estimates for evolving from the plant‐only to the plant‐litter system configuration suggest a pathogen would likely first have evolved the ability to reproduce in litter (colonized before the litter was shed, as live tissue); then later, the pathogen would have evolved the ability to colonize litter directly.

The relationship between equilibrium pathogen densities and transmission rates depends on how a plant host's size affects its own rate of biomass growth. Sometimes, pathogen abundance is maximal at intermediate transmission rates, suggesting a possible novel mechanism for emergence of a ‘prudent pathogen’ (a pathogen that exploits the host at a moderate, sustainable rate).

Synthesis . Our work elucidates when litter promotes—or inhibits—pathogen spread, underscores the consequences of different host biomass growth patterns for plant–pathogen dynamics, including a pathogen's ability to colonize a novel plant host, and suggests pathways by which different plant‐litter‐pathogen configurations might have evolved.