Soil Microbiomes Underlie Population Persistence of an Endangered Plant Species

David, Aaron S.; Quintana‐Ascencio, Pedro F.; Menges, Eric S.; Thapa‐Magar, Khum B.; Afkhami, Michelle E.; Searcy, Christopher A.

doi:10.1086/704684

Cited by 39 publications

(34 citation statements)

References 30 publications

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“…Rosemary scrub contains unique assemblages of herbaceous plant species, many of which are endemic to the habitat (Menges and Kohfeldt 1995). Environmental stress increases with elevation, as soil N and P, microbial abundance, and vegetation density generally decrease and soil drainage increases with higher elevation relative to the water table (Abrahamson et al 1984, David et al 2019D. Hernandez et al, unpublished manuscript).…”

Section: Study Systemmentioning

confidence: 99%

“…We grew individuals of 12 plant species in factorial experiments that manipulated the presence of microbes ("Live" vs. "Sterilized" conditions) in soils collected from nine patches at Archbold Biological Station. Patches were selected to span the range of elevations rosemary scrub occurs at, varying from 0.6 to 2.56 m above the boundary of the nearest mapped wetland (David et al 2019). Relative elevation is therefore an approximation of a patch's distance to the water table.…”

Section: Experimental Design and Setupmentioning

confidence: 99%

“…We manipulated the presence of soil microbes following David et al (2019). Briefly, we inoculated pots (15% soil volume) with Live (unmanipulated, microbially active) or Sterilized (autoclaved, microbially sterile) soils, with the remainder of the soil consisting of sterilized soil from the same rosemary scrub patch as the inoculum.…”

Section: Experimental Design and Setupmentioning

confidence: 99%

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Do plant–microbe interactions support the Stress Gradient Hypothesis?

David

Thapa‐Magar

Menges

et al. 2020

Ecology

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The Stress Gradient Hypothesis (SGH), which predicts increasing ratios of facilitative:competitive interactions with increasing stress, has long been a guiding framework for conceptualizing plant-plant interactions. Recently, there has been a growing recognition of the roles of microbes in mitigating or exacerbating environmental stress for their plant hosts. As such, we might predict, based on the SGH, that beneficial microbial effects on plant performance should be positively associated with stress. Specifically, we hypothesized that support for the SGH would depend on the host plant's habitat specialization such that species that specialize in high stress habitats and thus likely coevolved with the resident microbes would exhibit stronger support for the SGH than non-specialist plant species. We further hypothesized that support for the SGH would vary with germination frequency, since boosting germination of low-frequency germinators is one effective means by which microbes can benefit plant species performance. Here, we explore whether plant-microbial interactions support the SGH using 12 plant species native to the Florida rosemary scrub. We conducted factorial experiments that manipulated the presence of microbes in nine soils collected along an elevational stress gradient, and recorded germination frequency and biomass. Microbes increased the germination frequency of four species, all of which had relatively low germination rates. Furthermore, we found support for the SGH in nearly one-half of the species examined, with soil microbes facilitating germination with increasing stress for 5 of the 12 species tested, and none of the species exhibiting the opposite trend. Support for the SGH was not predicted by either the plant hosts' habitat specialization or germination frequency. In contrast to germination, biomass results showed little support for the SGH, with four of 12 species refuting and one species supporting SGH predictions. Taken together, our study documents that interactions between the soil microbial community and plant species along a stress gradient can support the SGH, but emphasizes that these effects are life-history-stage dependent. This work also identifies a common mechanism (germination facilitation) by which microbes can benefit plant species in stressful habitats.

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Section: Study Systemmentioning

confidence: 99%

Section: Experimental Design and Setupmentioning

confidence: 99%

Section: Experimental Design and Setupmentioning

confidence: 99%

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Do plant–microbe interactions support the Stress Gradient Hypothesis?

David

Thapa‐Magar

Menges

et al. 2020

Ecology

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“…However, population survival is highly dependent on interactions with other species. In particular, the fitness of plants and animals can be strongly influenced by interactions with their microbiomes, i.e., the bacteria, archaea, microeukaryotes and viruses that live on and inside of hosts, (David et al, ; Gould et al, ; Pillai, Gouhier, & Vollmer, ). Collectively, these microorganisms can affect host nutrition, behaviour, physiology, and development in various ways (Lynch & Hsiao, ).…”

Section: Microbial Rescue Effectsmentioning

confidence: 99%

Microbial rescue effects: How microbiomes can save hosts from extinction

et al. 2020

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Environmental change is occurring across the globe at an unprecedented rate. With atmospheric CO 2 concentrations now exceeding 400 ppm (Blunden, Arndt, & Hartfield, 2018), global mean surface temperatures are rising (Stocker et al., 2013) and the world ocean is becoming more acidic (Gattuso et al., 2015). Habitat is being degraded and homogenized via land-use change while nutrient runoff from industrial-scale agriculture is expanding anoxic dead zones in coastal ecosystems (Foley, 2005; Stocker et al., 2013). Meanwhile, altered precipitation regimes are creating more intense and prolonged periods of drought and flooding that threaten our ability to reliably feed the growing human population (Trenberth, 2011). These and other global changes pose severe threats to the biodiversity of virtually all ecosystems on Earth. For species to persist in the face of widespread and rapid environmental change, it is important to identify biological mechanisms that can reverse trends of population decline. Some populations can achieve this by moving into more favourable habitats, for example, through the migration of heat-stressed individuals to sites at higher latitudes with cooler temperatures (Chen,

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“…Large open gaps in recently burned Florida rosemary scrub patches are the most suitable habitat for H. cumulicola (Quintana‐Ascencio et al, , ) . Post‐fire, increasing shrub cover (Menges, Main, et al, ), decreasing moisture (Weekley, Gagnon, Menges, Quintana‐Ascencio, & Saha, ), varying nutrients (Schafer & Mack, ) and changing interactions with microbes (David et al, ) and other organisms (Brudvig & Quintana‐Ascencio, ) affect the vital rates and population growth of H. cumulicola . Dormancy and post‐fire germination (Dolan et al, ; Quintana‐Ascencio & Morales‐Hernandez, ) increase chances of taking advantage of the occurrence of more suitable recently burned habitats and seed dispersal allows reaching newly created post‐fire neighbouring suitable habitats.…”

Section: Discussionmentioning

confidence: 99%

Assessing the roles of seed bank, seed dispersal and historical disturbances for metapopulation persistence of a pyrogenic herb

et al. 2019

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1. Seed bank, seed dispersal and historical disturbance are critical factors affecting plant population persistence. However, because of difficulties collecting data on these factors they are often ignored.2. We evaluated the roles of seed bank, seed dispersal and historical disturbance on metapopulation persistence of Hypericum cumulicola, a Florida endemic. We took advantage of long-term demographic data of multiple populations (22 years; ~11 K individuals; 15 populations) and a wealth of information on burn history (1962present), and habitat attributes (patch specific location, elevation, area and aggregation) of a system of 92 patches of Florida rosemary scrub. We used previously developed integral projection models to assess the relative ability of simulations with different levels of seed dormancy for recently produced and older seeds and different dispersal kernels (including no dispersal) to predict regional observed occupancy and plant abundance in patches in 2016-2018. We compared a simulation with this model using historical burn history to 500 model simulations with the same average fire regime (using a Weibull distribution to determine the probability of ignition) but with random ignition years.3. The most likely model had limited dispersal (mean = 0.5 m) and the highest dormancy (field estimates × 1.2 %) and its predictions were associated with observed occurrences (67% correct) and densities (20% of variance explained). Historical burn synchrony among neighbouring patches (skewness in the number of patches burned by year = 1.79) probably explains the higher densities predicted by the simulation with the historical fire regime compared with predicted abundances after simulations using random ignition years (skewness = 0.20 + SE = 0.01). Synthesis.Our findings demonstrate the pivotal role of seed dormancy, dispersal and fire history on population dynamics, distribution and abundance. Because of the prevalence of metapopulation dynamics, we should be aware of the significance of changes in the availability and configuration of suitable habitat associated with human or non-human landscape changes. Decisions on prescribed fires (or other disturbances) will benefit from our knowledge of consequences of fire frequency, but also of location of ignition and the probability of fire spread.

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Soil Microbiomes Underlie Population Persistence of an Endangered Plant Species

Cited by 39 publications

References 30 publications

Do plant–microbe interactions support the Stress Gradient Hypothesis?

Do plant–microbe interactions support the Stress Gradient Hypothesis?

Microbial rescue effects: How microbiomes can save hosts from extinction

Assessing the roles of seed bank, seed dispersal and historical disturbances for metapopulation persistence of a pyrogenic herb

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