Disentangling the role of oomycete soil pathogens as drivers of plant-soil feedbacks

Abstract

Interactions among plant species and their soil biota drive plant-soil feedbacks (PSFs) that play a major role in the dynamics and diversity of plant communities. Among the different components of the soil community, pathogens are considered to be the main drivers of negative PSFs. Despite this, the number of studies that have experimentally quantified the contribution of soil pathogens to PSFs remains considerably low. Here we conducted a greenhouse experiment with oomycete-specific fungicide to quantify the contribution of soil pathogens, and particularly oomycete pathogens, to individual and pairwise PSFs in forest communities. We used as a case study Mediterranean mixed forests dominated by Quercus suber and invaded by the oomycete pathogen Phytophthora cinnamomi. The fungicide treatment was crossed with a competition treatment to explore how conspecific neighbors might modify pathogen effects. To place the results of the experiment in a wider context, we also conducted a systematic review of published papers that explicitly used fungicide to explore the role of pathogens in PSF experiments. Our experimental results showed that oomycete pathogens were the main drivers of individual PSFs in the study forests. Oomycete effects varied among tree species according to their susceptibility to P. cinnamomi, driving negative PSFs in the highly susceptible Q. suber but not in the coexistent Olea europaea. Oomycete-driven PSFs were not modified by intraspecific competition. Oomycete pathogens were also major contributors to negative pairwise PSFs assumed to promote species coexistence. Results from the systematic review supported the novelty of our experimental results, since only three studies had previously used oomycete-specific fungicide in a PSF context and none in systems invaded by exotic oomycetes. Overall, our results provide novel evidence of oomycete pathogens (including the exotic P. cinnamomi) as fundamental drivers of negative individual and pairwise PSFs with implications for species coexistence in invaded communities. Although in the short-term invasive pathogens might contribute to species coexistence by causing self-limitation in dominant species, strong inter-specific variation in self-limitation might undermine coexistence in the long-term. Because of the increasing number of exotic oomycetes worldwide, further attention should be given to oomycetes as drivers of PSFs in plant communities.

Keywords: Phytophthora cinnamomi; coexistence; exotic pathogens; oak decline; oomycete-specific fungicide; plant competition; plant-soil interactions; root traits.