Microbes are increasingly recognized as ubiquitous, hidden players that can dramatically affect the functioning of plants and animals as well as higher order biological processes such as community assembly, the maintenance of biodiversity, and ecosystem function, health, and stability. For example, many plants depend on microbial symbionts for nutrient acquisition and herbivore defense (i.e., mutualism), while other microbes are plant pathogens. Despite how commonly microbes influence individual-level plant fitness, our understanding of whether these effects scale up to impact population growth rates and persistence comes predominantly from studies of tightly coevolved, mutualistic fungi or studies that largely ignored vital rates critical to plant population persistence. Research investigating how diverse soil microbial communities affect plant population dynamics is therefore urgently needed to advance our understanding of how microbes influence plant population persistence and ultimately species distributions. Here, we use an integrative approach combining long term datasets (e.g.,28 years), manipulative experiments, and integral projection modeling to quantify 1) the effect microbes have on individual fitness of 12 plant species from the imperiled Florida scrub ecosystem and 2) the role these microbial effects play in maintaining populations or contributing to their decline.
In our experiments comparing plants grown on sterilized soil versus microbial-active soil, we observed significant effects of microbes on plant performance across the majority of species. For example, microbes significantly increased germination of three species, including two federally-listed plants (Hypericum cumulicola and Eryngium cunefolium), and significantly increased biomass of two species (both Fabaceae) and decreased biomass in three species. By integrating our individual-level results into demographic models, we found the first evidence for substantial effects of soil microbial communities on plant population growth rates. For instance, removal of microbes through soil sterilization led to a 50% reduction in germination (P<0.001) of the fire-dependent, federally-endangered herb Hypericum cumulicola and decreased the number of years post-fire with positive population growth (λ > 1) from 5 years with microbes to 3 years without microbes. We also found that anthropogenic changes, such as fire suppression, can reduce the importance of microbes for population growth and result in population declines of imperiled plant species. Overall, our results illustrate the importance of considering interactions with diverse soil microbial communities for understanding plant population dynamics and making informed conservation decisions for threatened species.