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.