American Society of Naturalists

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“Pathogens and mutualists as joint drivers of host species coexistence and turnover: implications for plant competition and succession”

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Jiang Jiang, Karen C. Abbott, Mara Baudena, Maarten B. Eppinga, James A. Umbanhowar, and James Bever (Apr 2020)

Pathogens and mutualists as joint drivers of host species coexistence and turnover

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In plant ecology, host-host interactions can be influenced by interactions with pathogens and mutualists. Recent studies have demonstrated that either a pathogen or a mutualist can generate a positive feedback and cause alternative stable states, and either may generate a negative feedback and promoting coexistence. However, the joint influence of both microbes on plant-plant interactions has rarely been studied. When pathogens and mutualists are both present, the potential for simultaneous positive and negative feedbacks can generate a wide range of possible effects on host species coexistence and turnover. This study uses a simple model to produce novel and surprising outcomes about the dynamics of plant-soil feedbacks and their consequences for host species competition and succession. The authors identify the conditions under which the joint actions of pathogens and mutualists can mediate coexistence. Interestingly, they find that a combination of positive and negative plant-microbe feedbacks could result in a coexistence state as an alternative stable state, alongside exclusion of some of the community members. The outcome may not be detectable through the typical design of experimental plant-soil feedback studies. The study provides guidance for empiricists to test these model predictions with a new type of pot experiment that independently and factorially manipulates components of plant microbiome. Such an experiment might evaluate plant fitness and competitive effects across a range of initial densities of two plant species factorially manipulated with the presence and timing of introduction of a pathogen and a mutualist.


Abstract

The potential for either pathogens or mutualists to alter the outcome of interactions between host species has been clearly demonstrated experimentally, but our understanding of their joint influence remains limited. Individually, pathogens and mutualists can each stabilize (via negative feedback) or destabilize (via positive feedback) host-host interactions. When pathogens and mutualist are both present, the potential for simultaneous positive and negative feedbacks can generate a wide range of possible effects on host species coexistence and turnover. Extending existing theoretical frameworks, we explore the range of dynamics generated by simultaneous interactions with pathogens and mutualists and identify the conditions for pathogen or mutualist mediation of host coexistence. We then explore the potential role of microbial mutualists and pathogens in plant species turnover during succession. We show how a combination of positive and negative plant-microbe feedbacks can generate a coexistence state that is part of a set of alternative stable states. This result implies that the outcomes of coexistence from classical plant-soil feedback experiments may be susceptible to disturbances, and that empirical investigations of microbially-mediated coexistence would benefit from consideration of interactive effects of feedbacks generated from different distinct components of the plant microbiome.