Rebecca L. McCulley

Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States.

Prairie Redux Tallgrass prairie is extinct across much of its former range in the midwestern United States, but relicts preserved in cemeteries and nature reserves allow functional comparison of former grassland soils with modern agricultural soils. Fierer et al. (p. 621; see the Perspective by Scholes and Scholes) took matched soil samples from sites representing the gamut of climate conditions and modeled the combination of genomic analysis and environmental data to resurrect the historical prairie soil communities, identifying the nutrient-scavenging Verrucomicrobia as keystone bacteria in functioning prairie. Analysis of microbiota in prairie soil relicts offers insights into the ecological function of a near-extinct biome. [Also see Perspective by Scholes and Scholes] Native tallgrass prairie once dominated much of the midwestern United States, but this biome and the soil microbial diversity that once sustained this highly productive system have been almost completely eradicated by decades of agricultural practices. We reconstructed the soil microbial diversity that once existed in this biome by analyzing relict prairie soils and found that the biogeographical patterns were largely driven by changes in the relative abundance of Verrucomicrobia, a poorly studied bacterial phylum that appears to dominate many prairie soils. Shotgun metagenomic data suggested that these spatial patterns were associated with strong shifts in carbon dynamics. We show that metagenomic approaches can be used to reconstruct below-ground biogeochemical and diversity gradients in endangered ecosystems; such information could be used to improve restoration efforts, given that even small changes in below-ground microbial diversity can have important impacts on ecosystem processes.

Grassland productivity limited by multiple nutrients

Terrestrial ecosystem productivity is widely accepted to be nutrient limited1. Although nitrogen (N) is deemed a key determinant of aboveground net primary production (ANPP)2,3, the prevalence of co-limitation by N and phosphorus (P) is increasingly recognized4–8. However, the extent to which terrestrial productivity is co-limited by nutrients other than N and P has remained unclear. Here, we report results from a standardized factorial nutrient addition experiment, in which we added N, P and potassium (K) combined with a selection of micronutrients (K+μ), alone or in concert, to 42 grassland sites spanning five continents, and monitored ANPP. Nutrient availability limited productivity at 31 of the 42 grassland sites. And pairwise combinations of N, P, and K+μ co-limited ANPP at 29 of the sites. Nitrogen limitation peaked in cool, high latitude sites. Our findings highlight the importance of less studied nutrients, such as K and micronutrients, for grassland productivity, and point to significant variations in the type and degree of nutrient limitation. We suggest that multiple-nutrient constraints must be considered when assessing the ecosystem-scale consequences of nutrient enrichment.

Abundance of introduced species at home predicts abundance away in herbaceous communities

Many ecosystems worldwide are dominated by introduced plant species, leading to loss of biodiversity and ecosystem function. A common but rarely tested assumption is that these plants are more abundant in introduced vs. native communities, because ecological or evolutionary-based shifts in populations underlie invasion success. Here, data for 26 herbaceous species at 39 sites, within eight countries, revealed that species abundances were similar at native (home) and introduced (away) sites - grass species were generally abundant home and away, while forbs were low in abundance, but more abundant at home. Sites with six or more of these species had similar community abundance hierarchies, suggesting that suites of introduced species are assembling similarly on different continents. Overall, we found that substantial changes to populations are not necessarily a pre-condition for invasion success and that increases in species abundance are unusual. Instead, abundance at home predicts abundance away, a potentially useful additional criterion for biosecurity programmes.

Conservation of nitrogen increases with precipitation across a major grassland gradient in the Central Great Plains of North America.

Regional analyses and biogeochemical models predict that ecosystem N pools and N cycling rates must increase from the semi-arid shortgrass steppe to the sub-humid tallgrass prairie of the Central Great Plains, yet few field data exist to evaluate these predictions. In this paper, we measured rates of net N mineralization, N in above- and belowground primary production, total soil organic matter N pools, soil inorganic N pools and capture in resin bags, decomposition rates, foliar 15N, and N use efficiency (NUE) across a precipitation gradient. We found that net N mineralization did not increase across the gradient, despite more N generally being found in plant production, suggesting higher N uptake, in the wetter areas. NUE of plants increased with precipitation, and δ15N foliar values and resin-captured N in soils decreased, all of which are consistent with the hypothesis that N cycling is tighter at the wet end of the gradient. Litter decomposition appeared to play a role in maintaining this regional N cycling trend: litter decomposed more slowly and released less N at the wet end of the gradient. These results suggest that immobilization of N within the plant–soil system increases from semi-arid shortgrass steppe to sub-humid tallgrass prairie. Despite the fact that N pools increase along a bio-climatic gradient from shortgrass steppe to mixed grass and tallgrass prairie, this element becomes relatively more limiting and is therefore more tightly conserved at the wettest end of the gradient. Similar to findings from forested systems, our results suggest that grassland N cycling becomes more open to N loss with increasing aridity.

Species abundance at home predicts abundance away in grasslands

Many ecosystems worldwide are dominated by introduced plant species, leading to loss of biodiversity and ecosystem function. A common but rarely tested assumption is that these plants are more abundant in introduced vs. native communities, because ecological or evolutionary-based shifts in populations underlie invasion success. Here, data for 26 herbaceous species at 39 sites, within eight countries, revealed that species abundances were similar at native (home) and introduced (away) sites - grass species were generally abundant home and away, while forbs were low in abundance, but more abundant at home. Sites with six or more of these species had similar community abundance hierarchies, suggesting that suites of introduced species are assembling similarly on different continents. Overall, we found that substantial changes to populations are not necessarily a pre-condition for invasion success and that increases in species abundance are unusual. Instead, abundance at home predicts abundance away, a potentially useful additional criterion for biosecurity programmes.

Effects of multiple climate change factors on the tall fescue–fungal endophyte symbiosis: infection frequency and tissue chemistry

• Climate change (altered CO(2) , warming, and precipitation) may affect plant-microbial interactions, such as the Lolium arundinaceum-Neotyphodium coenophialum symbiosis, to alter future ecosystem structure and function. • To assess this possibility, tall fescue tillers were collected from an existing climate manipulation experiment in a constructed old-field community in Tennessee (USA). Endophyte infection frequency (EIF) was determined, and infected (E+) and uninfected (E-) tillers were analysed for tissue chemistry. • The EIF of tall fescue was higher under elevated CO(2) (91% infected) than with ambient CO(2) (81%) but was not affected by warming or precipitation treatments. Within E+ tillers, elevated CO(2) decreased alkaloid concentrations of both ergovaline and loline, by c. 30%; whereas warming increased loline concentrations 28% but had no effect on ergovaline. Independent of endophyte infection, elevated CO(2) reduced concentrations of nitrogen, cellulose, hemicellulose, and lignin. • These results suggest that elevated CO(2) , more than changes in temperature or precipitation, may promote this grass-fungal symbiosis, leading to higher EIF in tall fescue in old-field communities. However, as all three climate factors are likely to change in the future, predicting the symbiotic response and resulting ecological consequences may be difficult and dependent on the specific atmospheric and climatic conditions encountered.

Forages and pastures symposium: fungal endophytes of tall fescue and perennial ryegrass: pasture friend or foe?

Tall fescue [Lolium arundinaceum (Schreb.) Darbysh. syn. Festuca arundinacea Schreb.] and perennial ryegrass (Lolium perenne L.) are important perennial forage grasses utilized throughout the moderate- to high-rainfall temperate zones of the world. These grasses have coevolved with symbiotic fungal endophytes (Epichloë/Neotyphodium spp.) that can impart bioactive properties and environmental stress tolerance to the grass compared with endophyte-free individuals. These endophytes have proven to be very important in pastoral agriculture in the United States, New Zealand, and Australia, where forage grasses are the principal feed for grazing ruminants. In this review, we describe the biology of these grass-endophyte associations and implications for the livestock industries that are dependent on these forages. Endophyte alkaloid production is put in context with endophyte diversity, and we illustrate how this has facilitated utilization of grasses infected with different endophyte strains that reduce livestock toxicity issues. Utilization of tall fescue and use of perennial ryegrass in the United States, New Zealand, and Australia are compared, and management strategies focused predominantly on the success of endophyte-infected perennial ryegrass in New Zealand and Australia are discussed. In addition, we consider the impact of grass-endophyte associations on the sustainability of pasture ecosystems and their likely response to future changes in climate.

Predicting the responsiveness of soil biodiversity to deforestation: a cross‐biome study

The consequences of deforestation for aboveground biodiversity have been a scientific and political concern for decades. In contrast, despite being a dominant component of biodiversity that is essential to the functioning of ecosystems, the responses of belowground biodiversity to forest removal have received less attention. Single-site studies suggest that soil microbes can be highly responsive to forest removal, but responses are highly variable, with negligible effects in some regions. Using high throughput sequencing, we characterize the effects of deforestation on microbial communities across multiple biomes and explore what determines the vulnerability of microbial communities to this vegetative change. We reveal consistent directional trends in the microbial community response, yet the magnitude of this vegetation effect varied between sites, and was explained strongly by soil texture. In sandy sites, the difference in vegetation type caused shifts in a suite of edaphic characteristics, driving substantial differences in microbial community composition. In contrast, fine-textured soil buffered microbes against these effects and there were minimal differences between communities in forest and grassland soil. These microbial community changes were associated with distinct changes in the microbial catabolic profile, placing community changes in an ecosystem functioning context. The universal nature of these patterns allows us to predict where deforestation will have the strongest effects on soil biodiversity, and how these effects could be mitigated.

Soil–Litter Mixing Accelerates Decomposition in a Chihuahuan Desert Grassland

Decomposition models typically under-predict decomposition relative to observed rates in drylands. This discrepancy indicates a significant gap in our mechanistic understanding of carbon and nutrient cycling in these systems. Recent research suggests that certain drivers of decomposition that are often not explicitly incorporated into models (for example, photodegradation and soil–litter mixing; SLM) may be important in drylands, and their exclusion may, in part, be responsible for model under-predictions. To assess the role of SLM, litterbags were deployed in the Chihuahuan Desert and interrelationships between vegetation structure, SLM, and rates of decomposition were quantified. Vegetation structure was manipulated to simulate losses of grass cover from livestock grazing and shrub encroachment. We hypothesized that reductions in grass cover would promote SLM and accelerate mass loss by improving conditions for microbial decomposition. Litter mass decreased exponentially, with the greatest losses occurring in concert with summer monsoons. There were no differences in decay constants among grass cover treatments. A significant, positive relationship between mass loss and SLM was observed, but contrary to expectations SLM was independent of grass cover. This suggests that processes operating at finer spatial scales than those in our grass removal treatments were influencing SLM. Shifts in litter lipid composition suggest increased bacterial contribution to decomposition through time. SLM, which is seldom included as a variable controlling decomposition in statistical or mechanistic models, was a strong driver of decomposition. Results are discussed in the context of other known drivers of decomposition in drylands (for example, UV radiation and climate) and more mesic systems.

Fungal endophyte presence and genotype affect plant diversity and soil-to-atmosphere trace gas fluxes

AimsNovel fungal endophyte (Neotyphodium coenophialum; Latch, Christensen and Samuels; Glenn, Bacon, and Hanlin) genotypes in symbiosis with tall fescue (Lolium arundinaceum; Schreb. Darbysh.) have been recently introduced to agricultural seed markets. These novel endophytes do not produce the full suite of toxins that the ‘common toxic’ form does, and therefore, may not have the same consequences on plant and soil processes. Here, we evaluated the effects of endophyte presence and genotype on ecosystem processes of tall fescue stands.MethodsWe quantified the effects of the presence of the common toxic endophyte (CT), two novel endophyte genotypes (AR-542, AR-584), no endophyte (endophyte free, E-), and a mixture of all endophyte statuses (mix) within a single genotype of tall fescue (PDF) on various soil and plant parameters.ResultsEndophyte presence and genotype affected tall fescue cover and plant species diversity: cover—CT, AR-542, AR -584, mix > E- and species diversity—E- > AR-542, AR -584 > CT, mix. Most measured soil parameters had significant endophyte effects. For example, higher fluxes of soil CO2 and N2O were measured from stands of AR-542 than from the other endophyte treatments.ConclusionsThese results indicate that endophyte presence and genetic identity are important in understanding the ecosystem-scale effects of this agronomically important grass-fungal symbiosis.