DISCUSSION
Our experiment revealed that soil pathogens accumulated more in exotic-dominated communities and, on average, those pathogens tended to be more generalist than those supported by plants in native-dominated communities. We observed a pattern of pathogen sharing congruent with asymmetric spillover, whereby native plants shared more pathogens with exotics than with other natives. Moreover, exotic plants showed strong potential to indirectly affect co-occurring native plants by spreading pathogens, whereas native plants had less influence over shared pathogen interactions. This asymmetric influence and sharing of generalist soil-borne pathogens from exotic to native plants correlated with impacts of exotics on native plants, suggesting that pathogen sharing had disproportionate impacts on native plant performance. These findings suggest that generalist fungal pathogens may constitute a feedback that increases exotic plant dominance in mixed communities of native and exotic plants.
Host richness and diversity can strongly influence disease dynamics (Susi et al. 2020), but our results suggest a stronger role of species identity, and more specifically, of provenance. Pathogen transmission is predicted to be lower in diverse communities (Mitchellet al. 2002), where pathogen abundance decreases via the dilution effect when suitable hosts occur at low abundance (Ostfeld & Keesing 2000). However, there is also evidence to suggest that more diverse plant communities can have higher pathogen densities as a result of amplification of generalists (i.e. pathogens that don’t respond to host density) (Power & Mitchell 2004; Halliday et al . 2017), particularly in plant communities containing fast-growing, less defended species (Cappelli et al. 2020). Our communities were all planted with the same initial plant richness, but native plants amplified more specialist pathogens in communities where they grew exclusively, whereas exotic plants amplified more generalists wherever they occurred. This difference appeared to have consequences for plant richness in communities, as plant richness was largely maintained to the end of the experiment in native communities, but declined sharply in exotic-dominated communities (reported in Waller et al. 2020). Our results suggest that declines in richness in exotic-dominated communities were due to increases in abundance of generalist pathogens that were amplified by exotic hosts, leading to apparent competition driving native biomass declines or mortality.
This study underscores the importance of conducting simultaneous plant-soil feedback experiments on plants grown alone and in communities, paired with characterization of the microbial communities. When grown in the monoculture feedback experiment, exotic plants were suppressed by soil previously inhabited by themselves, but this soil-mediated inhibition disappeared when these plants were grown in communities where they shared root pathogens. Viewed in isolation, and without the fungal community analysis, results from the monoculture experiment would suggest that specialist soil biota confers biotic resistance against exotic plants. However, when viewed in a community context, it appears more likely that sharing of generalist pathogens contributes to the competitive exclusion of natives by exotics, as a higher degree of pathogen sharing between exotic and native plants correlated with exotic impact in mixed communities. These results support a previous modeling study showing that exotic plants that accumulate generalist pathogens can spread and displace native plants, conditional on native fitness being more strongly affected by pathogens than the exotics (Eppinga 2006). More broadly, the divergent findings between the monoculture and community-level experiments may help explain why greenhouse plant-soil feedback experiments do not always translate into what is observed in the field (Heinze et al. 2016; Foreroet al. 2019).
Our findings indicate that exotic plants are amplifying and spreading generalist pathogens that are present in communities, resulting in reduced native plant success. We cannot determine whether the pathogen sharing between native and exotic plants constituted co-introduced non-native pathogens (“spillover”, e.g. Bufford et al. 2016) or native pathogens (“spillback”, e.g. Levine et al. 2004; Boreret al. 2007), as we do not know the provenance of the pathogens in this study. Either scenario can increase exotic plant success (Power & Mitchell 2004; Dickie et al. 2017), though spillback may be more common in plant invasions (Strauss et al. 2012). Indeed, many introduced plants experience a short-term release from pathogens in their newly introduced range (Mitchell & Power 2003), but begin to accumulate pathogens in their new range anywhere from 50-200 years after introduction (Hawkes 2007; Diez et al. 2010; Sikes et al. 2018). However, a high proportion of global pathogens are non-native to the area where they are recorded (Pimental 2001; Rua et al. 2011), so it would not be unreasonable to assume that many of the pathogens from our experiment were non-native.
Exotic plant invasions threaten biodiversity and ecosystem functions worldwide (Mack et al. 2000). Understanding how some invaders come to dominate native systems is therefore crucial to mitigating their impacts. Our results indicate that exotic plants benefit from fungal pathogen accumulation via disproportionate pathogen sharing with native plants.