American Society of Naturalists

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“Soil microbiomes underlie population persistence of an endangered plant species”

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Aaron S. David, Pedro F. Quintana-Ascencio, Eric S. Menges, Khum B. Thapa-Magar, Michelle E. Afkhami, and Christopher A. Searcy (Oct 2019)

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Bioassays, long-term demographic data, and integral projection modeling show soil microbiomes boost plant populations

<i>Hypericum cumulicola</i> in bloom.<br />(Credit: Pedro Quintana-Ascencio)
Hypericum cumulicola in bloom.
(Credit: Pedro Quintana-Ascencio)

Microbiomes can have profound effects on their hosts, yet we are still learning about their effects on higher-order processes. While recent research has considered how microbiomes alter processes at the community and ecosystem levels, lost in the shuffle has been the microbiome’s effect on host species’ populations, a knowledge gap that could have serious implications for plant and animal species listed as threatened and endangered.

The origins of this study began 25 years ago with the first censuses of the endangered Hypericum cumulicola, a perennial herb endemic to the imperiled Florida scrub ecosystem. Using detailed demographic data collected annually from 15 populations at Archbold Biological Station, along with spatial and historical factors such as fire history, elevation, patch aggregation, and patch size, an integral projection model (IPM) was developed that quantified H. cumulicola population dynamics across the landscape (Quintana-Ascencio et al. 2018 Journal of Ecology). Because of the flexibility built into this original population model, it would serve as an ideal tool to quantify how other factors, namely the soil microbiome, could influence population growth of the plant, provided that the effects of the soil microbiome on individual plants could be quantified.

<i>Hypericum cumulicola</i> in bloom.<br />(Credit: Reed Bowman)
Hypericum cumulicola in bloom.
(Credit: Reed Bowman)

In this new study, the authors set out to do just that by conducting bioassays that quantified the effect of microbes on two demographic rates critical to H. cumulicola populations – seed germination and first-year growth. By comparing the effects of live and sterilized soils on these demographic rates, they found that microbes substantially increased seed germination rates. Next, the authors incorporated the results of these bioassays into the IPM to quantify the population-level effects of the soil microbiome. The results were striking – in the absence of a soil microbiome, H. cumulicola populations would rarely experience population growth, leading to the conclusion that the soil microbiome plays a critical role in maintaining population persistence of its endangered host.


Abstract

Microbiomes can dramatically alter individual plant performance, yet how these effects influence higher order processes is not well resolved. In particular, little is known about how microbiome effects on individual plants alter plant population dynamics, a question critical to imperiled species conservation. Here, we integrate bioassays, multidecadal demographic data, and integral projection modeling to determine how the presence of the natural soil microbiome underlies plant population dynamics. Simulations indicated that the presence of soil microbiomes boosted population growth rates (λ) of the endangered Hypericum cumulicola by 13% on average, the difference between population growth versus decline in 76% of patches. The greatest benefit (47% increase in λ) occurred in low nutrient, high elevation habitats, suggesting that the soil microbiome may help expand H. cumulicola’s distribution to include these stressful habitats. Our results demonstrate that soil microbiomes can significantly affect plant population growth and persistence, and support the incorporation of soil microbiomes into conservation planning.