INTRODUCTION
Pathogenic microorganisms have considerable influence over species distributions (Dinoor & Eshed 1984; Bever 2015). Pathogens can disrupt plant communities by reducing the abundance of susceptible hosts, thereby benefitting those that are less susceptible in the community (Power & Mitchell 2004; Mordecai 2011). In invaded communities, exotic plant species can benefit when they support and tolerate a high abundance of generalist pathogens that are shared with native species (i.e. Accumulation of Local Pathogens Hypothesis, Eppinga 2006; Boreret al. 2007; Mitchell et al. 2010), resulting in pathogen-mediated apparent competition between plants (Holt 1977; Holt 2017, also known as disease-mediated invasion, Strauss et al.2012). Yet, the relative importance of pathogen accumulation in invaded communities and the means of pathogen spread via exotic hosts are difficult to quantify experimentally, and mark an important gap in our knowledge of plant community dynamics (Goss et al. 2020).
Plant hosts vary widely in their capacity to amplify and transmit pathogens (Paull et al. 2012). Asymptomatic or mildly symptomatic ‘amplification hosts’ (also known as reservoir hosts) can significantly disrupt natural communities by transmitting disease (Cronin et al. 2010). Several successful exotic plant hosts are known to accumulate pathogens that spill over onto native plants and suppress their growth (Malmstrom et al. 2005; Strauss et al. 2012), but the generality of this phenomenon is unknown. By contrast, exotic plants can have a neutral effect on pathogen abundance, or decrease it via the dilution effect (i.e. lower proportion of suitable hosts in the community, Ostfeld & Keesing 2000; Keesing, Holt & Ostfeld 2006) if they escape pathogens (i.e. Enemy Release Hypothesis, Keane & Crawley 2002) or are suppressed more than native plants (Stricker et al.2016). Understanding whether exotic plants amplify or dilute generalist pathogens in a community is key to understanding whether or not disease-mediated invasion may occur.
Exotic plants are likely to act as amplification hosts for several reasons. First, many exotic plants have “quick-return” strategies (i.e. faster growth, high nitrogen in tissues, Leishman et al.2007; van Kleunen et al. 2010) and are more competent hosts for antagonists, including pathogens, than “slow-return” species (Strauss & Agrawal 1999; Cronin et al. 2010; Cappelli et al. 2020; Allen et al. 2021). Second, many invasive plants tolerate damage from enemies with minimal impact on plant fitness (Roy & Kirchner 2000; Ashton & Lerdau 2008; Goss et al. 2020), and/or can replace tissues lost to enemies faster than slow-growing species (Gianoli & Salgado-Luarte 2017; Allen et al. 2021). Third, exotic plants can occur at high abundance locally, increasing pathogen establishment and spread opportunities (Burdon & Chilvers 1982; Gilbert 2002). Thus, maximum transmission rates by pathogens may occur in communities where the majority of biomass is made up of tolerant, exotic hosts (Parker & Gilbert 2004). Because many exotic, invasive plants possess quick-return strategies, are disease-tolerant, and occur at high abundance, they likely meet these criteria to act as amplification hosts.
Identifying amplification hosts in a multi-host, multi-pathogen system has proven challenging (Paull et al. 2012). Despite evidence that many plant pathogens are generalists and infect multiple hosts in the community (Parker and Gilbert 2007), interactions between plants and pathogens are typically studied in isolation of the wider community (but see Hawksworth 2001). Studies that do take a microbial community approach often use plant-soil feedbacks (Bever et al. 1997), comparing how plants differ in their influence on and response to pathogen communities in soils. However, plant-soil feedback experiments rarely use more than 1-2 plant hosts or characterize specific microbial functional groups, thereby failing to address whether effects of soil biota are due to pathogens or parasitic mutualists (e.g. mycorrhizal fungi, Klironomos 2003). Further, these tests cannot distinguish between the Enemy Release vs. Accumulation of Local Pathogens Hypotheses, because the absence of a growth depression from antagonistic soil biotic communities could mean that plants have either escaped or are simply tolerating accumulated pathogens. Finally, it is unclear whether plant-soil feedback effects observed in monoculture translate to a community, where sharing of interaction partners may produce influential indirect interactions (Allen 2020).
To test whether exotic plants accumulate generalist pathogens that spill over on to native plants, we characterized fungal pathogen communities in the roots of native and exotic plants growing together in 8-species communities (n=80) ranging in exotic dominance from 0-100%. We focus on soil-borne fungi, as these are the most common and aggressive pathogen group affecting plants (Delgado-Baquerizo et al. 2020). We quantified the degree of sharing between native and exotic plant hosts by calculating the proportion of OTUs shared, the generality of associations of both plants and fungi (relative to other species in the community), and the frequency at which generalists are shared with other plants. We also conducted a single-species plant-soil feedback experiment with the plant species and compared their responses to those in the community-level experiment, where we also included a plant-soil feedback treatment. We addressed the following research questions: 1) Do exotic plants accumulate generalist fungal taxa that are known to cause plant disease (i.e. putative pathogens)? 2) Given their higher generalism, do exotic plants share a greater proportion of fungal pathogens with natives than do other native plants? 3) Does feedback between exotic plants and putatively pathogenic fungal taxa explain exotic plant success alone and in plant communities? And 4) Do plant-soil feedbacks in monoculture predict feedbacks in a community? Our results show that exotic plants are more generalist in their associations compared with natives, driving asymmetric spillover of pathogens from exotic to native plants compared to null expectation, which correlates with exotic plant success in communities but not monoculture.