Consistent predictors of microbial community composition across spatial scales in grasslands reveal low context-dependency.

Environmental circumstances shaping soil microbial communities have been studied extensively. However, due to disparate study designs, it has been difficult to resolve whether a globally consistent set of predictors exists, or context-dependency prevails. Here, we used a network of 18 grassland sites (11 of those containing regional plant productivity gradients) to examine (i) if similar abiotic or biotic factors predict both large-scale (across sites) and regional-scale (within sites) patterns in bacterial and fungal community composition, and (ii) if microbial community composition differs consistently at two levels of regional plant productivity (low vs. high). Our results revealed that bacteria were associated with particular soil properties (such as base saturation) and both bacteria and fungi were associated with plant community composition across sites and within the majority of sites. Moreover, a discernible microbial community signal emerged, clearly distinguishing high and low-productivity soils across different grasslands independent of their location in the world. Hence, regional productivity differences may be typified by characteristic soil microbial communities across the grassland biome. These results could encourage future research aiming to predict the general effects of global changes on soil microbial community composition in grasslands and to discriminate fertile from infertile systems using generally applicable microbial indicators.

Relative importance of competition and plant-soil feedback, their synergy, context dependency and implications for coexistence.

Plants interact simultaneously with each other and with soil biota, yet the relative importance of competition vs. plant-soil feedback (PSF) on plant performance is poorly understood. Using a meta-analysis of 38 published studies and 150 plant species, we show that effects of interspecific competition (either growing plants with a competitor or singly, or comparing inter- vs. intraspecific competition) and PSF (comparing home vs. away soil, live vs. sterile soil, or control vs. fungicide-treated soil) depended on treatments but were predominantly negative, broadly comparable in magnitude, and additive or synergistic. Stronger competitors experienced more negative PSF than weaker competitors when controlling for density (inter- to intraspecific competition), suggesting that PSF could prevent competitive dominance and promote coexistence. When competition was measured against plants growing singly, the strength of competition overwhelmed PSF, indicating that the relative importance of PSF may depend not only on neighbour identity but also density. We evaluate how competition and PSFs might interact across resource gradients; PSF will likely strengthen competitive interactions in high resource environments and enhance facilitative interactions in low-resource environments. Finally, we provide a framework for filling key knowledge gaps and advancing our understanding of how these biotic interactions influence community structure.

Toward more robust plant-soil feedback research.

Understanding if and how plant-soil biota feedbacks (PSFs) shape plant communities has become a major research priority. In this paper, we draw on a recent, high-profile PSF study to illustrate that certain widely used experimental methods cannot reliably determine if PSFs occur. One problem involves gathering soil samples adjacent to multiple conditioning plants, mixing the samples and then growing phytometers in the mixtures to test for PSFs. This mixed soil approach does not establish that the conditioning plant being present caused the soil biota to be present, the first step of a PSF. Also, soil mixing approximates replacing raw data with averages prior to analysis, a move certain to generate falsely precise statistical estimates. False precision also results from sample sizes being artificially inflated when phytometers are misinterpreted as experimental units. Plant biomass ratios become another source of false precision when individual plant values contribute to multiple ratio observations. Any one of these common missteps can cause still living null hypotheses to be pronounced dead, and risks of this increase with numbers of missteps. If soil organisms truly structure plant communities, then null hypotheses indicating otherwise will not survive proper testing. We discuss conceptual, experimental and analytical refinements to facilitate accurate testing.

Plant functional traits and phylogenetic relatedness explain variation in associations with root fungal endophytes in an extreme arid environment.

Since root endophytes may ameliorate drought stress, understanding which plants associate with endophytes is important, especially in arid ecosystems. Here, the root endophytes were characterized of 42 plants from an arid region of Argentina. Colonization by arbuscular mycorrhizal fungi (AMF) and dark septate endophytes (DSEs) was related to plant functional type (PFT), family, and phylogenetic relatedness. Overall, three main findings were observed. Firstly, only moderate levels of endophyte associations were found across all taxa (e.g., most Poaceae were not colonized by endophytes despite numerous accounts of colonization by AMF and DSEs). We determined 69% of plant taxa associated with some form of root endophyte but levels were lower than other regional studies. Secondly, comparisons by PFT and phylogeny were often qualitatively similar (e.g., succulents and Portulacineae consistently lacked AMF; variation occurred among terrestrial vs. epiphytic bromeliads) and often differed from comparisons based on plant family. Thirdly, comparisons by plant family often failed to account for important variation either within families (e.g., Bromeliaceae and Poaceae) or trait conservatism among related families (i.e., Rosidae consistently lacked DSEs and Portulacineae lacked AMF). This study indicates the value of comparing numerous taxa based on PFTs and phylogenetic similarity. Overall, the results suggest an uncertain benefit of endophytes in extremely arid environments where plant traits like succulence may obviate the need to establish associations.

Phylogenetic conservatism in plant-soil feedback and its implications for plant abundance.

We examined whether plant-soil feedback and plant-field abundance were phylogenetically conserved. For 57 co-occurring native and exotic plant species from an old field in Canada, we collected a data set on the effects of three soil biota treatments on plant growth: net whole-soil feedback (combined effects of mutualists and antagonists), feedback with arbuscular mycorrhizal fungi (AMF) collected from soils of conspecific plants, and feedback with Glomus etunicatum, a dominant mycorrhizal fungus. We found phylogenetic signal in both net whole-soil feedback and feedback with AMF of conspecifics; conservatism was especially strong among native plants but absent among exotics. The abundance of plants in the field was also conserved, a pattern underlain by shared plant responses to soil biota. We conclude that soil biota influence the abundance of close plant relatives in nature.

Predicting plant responses to mycorrhizae: integrating evolutionary history and plant traits.

We assessed whether (1) arbuscular mycorrhizal colonization of roots (RC) and/or plant responses to arbuscular mycorrhizae (MR) vary with plant phylogeny and (2) MR and RC can be more accurately predicted with a phylogenetic predictor relative to a null model and models with plant trait and taxonomic predictors. In a previous study, MR and RC of 95 grassland species were measured. We constructed a phylogeny for these species and found it explained variation in MR and RC. Next, we used multiple regressions to identify the models that most accurately predicted plant MR. Models including either phylogenetic or phenotypic and taxonomic information similarly improved our ability to predict MR relative to a null model. Our study illustrates the complex evolutionary associations among species and constraints of using phylogenetic information, relative to plant traits, to predict how a plant species will interact with AMF.

The organization of plant communities: negative plant-soil feedbacks and semiarid grasslands.

Understanding how plant communities are organized requires uncovering the mechanism(s) regulating plant species coexistence and relative abundance. Negative soil feedbacks may affect plant communities by suppressing dominant species, causing rarity of most plants, or reducing the competitive abilities of all species. Here, three soil feedback experiments were used to differentiate the effects of soil feedbacks on mid- to late-successional and semiarid grasslands. Then I tested whether the direction and degree of soil feedback accounts for variation in relative abundance among species that coexist within each plant community. Negative soil feedbacks predominated across all species and sites and were individually discernible for 40% of plant species. Negative soil feedbacks affected rare to dominant plant species. Negative soil feedbacks, capable of having negative frequency-dependent effects, have the potential to act as a fundamental driver of species coexistence.

Effects of soil biota from different ranges on Robinia invasion: acquiring mutualists and escaping pathogens.

The net effects of soil biota on exotic invaders can be variable, in part, because net effects are produced by many interacting mutualists and antagonists. Here we compared mutualistic and antagonistic biota in soils collected in the native, expanded, and invasive range of the black locust tree, Robinia pseudoacacia. Robinia formed nodules in all soils with a broad phylogenetic range of N-fixing bacteria, and leaf N did not differ among the different sources of soil. This suggests that the global expansion of Robinia was not limited by the lack of appropriate mutualistic N-fixers. Arbuscular mycorrhizal fungi (AMF) from the native range stimulated stronger positive feedbacks than AMF from the expanded or invasive ranges, a biogeographic difference not described previously for invasive plants. Pythium taxa collected from soil in the native range were not more pathogenic than those from other ranges; however, feedbacks produced by the total soil biota were more negative from soils from the native range than from the other ranges, overriding the effects of AMF. This suggests that escape from other pathogens in the soil or the net negative effects of the whole soil community may contribute to superior performance in invaded regions. Our results suggest that important regional evolutionary relationships may occur among plants and soil biota, and that net effects of soil biota may affect invasion, but in ways that are not easily explained by studying isolated components of the soil biota.

Globally, plant-soil feedbacks are weak predictors of plant abundance.

Plant-soil feedbacks (PSFs) have been shown to strongly affect plant performance under controlled conditions, and PSFs are thought to have far reaching consequences for plant population dynamics and the structuring of plant communities. However, thus far the relationship between PSF and plant species abundance in the field is not consistent. Here, we synthesize PSF experiments from tropical forests to semiarid grasslands, and test for a positive relationship between plant abundance in the field and PSFs estimated from controlled bioassays. We meta-analyzed results from 22 PSF experiments and found an overall positive correlation (0.12 ≤  r ¯  ≤ 0.32) between plant abundance in the field and PSFs across plant functional types (herbaceous and woody plants) but also variation by plant functional type. Thus, our analysis provides quantitative support that plant abundance has a general albeit weak positive relationship with PSFs across ecosystems. Overall, our results suggest that harmful soil biota tend to accumulate around and disproportionately impact species that are rare. However, data for the herbaceous species, which are most common in the literature, had no significant abundance-PSFs relationship. Therefore, we conclude that further work is needed within and across biomes, succession stages and plant types, both under controlled and field conditions, while separating PSF effects from other drivers (e.g., herbivory, competition, disturbance) of plant abundance to tease apart the role of soil biota in causing patterns of plant rarity versus commonness.

Virulence of soil-borne pathogens and invasion by Prunus serotina.

*Globally, exotic invaders threaten biodiversity and ecosystem function. Studies often report that invading plants are less affected by enemies in their invaded vs home ranges, but few studies have investigated the underlying mechanisms. *Here, we investigated the variation in prevalence, species composition and virulence of soil-borne Pythium pathogens associated with the tree Prunus serotina in its native US and non-native European ranges by culturing, DNA sequencing and controlled pathogenicity trials. *Two controlled pathogenicity experiments showed that Pythium pathogens from the native range caused 38-462% more root rot and 80-583% more seedling mortality, and 19-45% less biomass production than Pythium from the non-native range. DNA sequencing indicated that the most virulent Pythium taxa were sampled only from the native range. The greater virulence of Pythium sampled from the native range therefore corresponded to shifts in species composition across ranges rather than variation within a common Pythium species. *Prunus serotina still encounters Pythium in its non-native range but encounters less virulent taxa. Elucidating patterns of enemy virulence in native and nonnative ranges adds to our understanding of how invasive plants escape disease. Moreover, this strategy may identify resident enemies in the non-native range that could be used to manage invasive plants.

Spatial variation in soil-borne disease dynamics of a temperate tree, Prunus serotina.

Soil-borne pathogens are posited to maintain forest diversity. However, their in situ impact and spatial variation are largely unknown. We examined spatial patterns of pathogenic activity in a deciduous forest using a common garden experiment and also in a natural experiment around replicated trees, and we quantified Pythium (a soil-borne pathogen) density around individual Prunus serotina trees. In both experiments, P. serotina seedling survival was 52-57% greater in plots treated with a metalaxyl-based fungicide specific to oomycetes (i.e., Pythium) than in untreated plots. Disease dynamics were not density dependent, but pathogenic activity and Pythium density were spatially variable. In the common garden and natural experiments, pathogenic activity of soil inoculum varied among trees, while in the natural experiment disease dynamics were also distance dependent and pathogenic activity decreased away from P. serotina trees. Disease and Pythium density were not always related but displayed considerable spatial variation. We found that Pythium density did not vary with distance away from P. serotina trees but did vary among trees. Understanding the spatial complexity of soil-borne pathogens is critical to accurately characterizing their effects on populations and ultimately on forest diversity.

Does responsiveness to arbuscular mycorrhizal fungi depend on plant invasive status?

Differences in the direction and degree to which invasive alien and native plants are influenced by mycorrhizal associations could indicate a general mechanism of plant invasion, but whether or not such differences exist is unclear. Here, we tested whether mycorrhizal responsiveness varies by plant invasive status while controlling for phylogenetic relatedness among plants with two large grassland datasets. Mycorrhizal responsiveness was measured for 68 taxa from the Northern Plains, and data for 95 taxa from the Central Plains were included. Nineteen percent of taxa from the Northern Plains had greater total biomass with mycorrhizas while 61% of taxa from the Central Plains responded positively. For the Northern Plains taxa, measurable effects often depended on the response variable (i.e., total biomass, shoot biomass, and root mass ratio) suggesting varied resource allocation strategies when roots are colonized by arbuscular mycorrhizal fungi. In both datasets, invasive status was nonrandomly distributed on the phylogeny. Invasive taxa were mainly from two clades, that is, Poaceae and Asteraceae families. In contrast, mycorrhizal responsiveness was randomly distributed over the phylogeny for taxa from the Northern Plains, but nonrandomly distributed for taxa from the Central Plains. After controlling for phylogenetic similarity, we found no evidence that invasive taxa responded differently to mycorrhizas than other taxa. Although it is possible that mycorrhizal responsiveness contributes to invasiveness in particular species, we find no evidence that invasiveness in general is associated with the degree of mycorrhizal responsiveness. However, mycorrhizal responsiveness among species grown under common conditions was highly variable, and more work is needed to determine the causes of this variation.

Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics.

Feedback with soil biota is an important determinant of terrestrial plant diversity. However, the factors regulating plant-soil feedback, which varies from positive to negative among plant species, remain uncertain. In a large-scale study involving 55 species and 550 populations of North American trees, the type of mycorrhizal association explained much of the variation in plant-soil feedbacks. In soil collected beneath conspecifics, arbuscular mycorrhizal trees experienced negative feedback, whereas ectomycorrhizal trees displayed positive feedback. Additionally, arbuscular mycorrhizal trees exhibited strong conspecific inhibition at multiple spatial scales, whereas ectomycorrhizal trees exhibited conspecific facilitation locally and less severe conspecific inhibition regionally. These results suggest that mycorrhizal type, through effects on plant-soil feedbacks, could be an important contributor to population regulation and community structure in temperate forests.

Invasion through quantitative effects: intense shade drives native decline and invasive success.

The effects of invasive nonnative species on community composition are well documented. However, few studies have determined the mechanisms by which invaders drive these changes. The literature indicates that many nonnative plant species alter light availability differently than natives in a given community, suggesting that shading may be such a mechanism. We compared light quantity (photosynthetically active radiation, PAR) and quality (red: far-red ratio, R:Fr) in riparian reaches heavily invaded by a nonnative tree (Acer platanoides) to that in an uninvaded forest and experimentally tested the effects of our measured differences in PAR and R:Fr on the survival, growth, and biomass allocation of seedlings of the dominant native species and Acer platanoides. Light conditions representative of the understory of Acer platanoides-invaded forest decreased survival of the native maple Acer glabrum by 28%; Amelanchier alnifolia by 32%; Betula occidentalis by 55%; Elymus glaucus by 46%; and Sorbus aucuparia by 52%, relative to seedlings growing in PAR similar to that of native understories. In contrast, Acer platanoides and the native shrub Symphoricarpos albus were not affected by reductions in PAR. Acer platanoides seedlings and saplings are uniquely adapted to shade relative to native species. Acer platanoides was the only species tested that decreased allocation to roots relative to shoots in the invaded forest vs. the native forest light conditions. Therefore it was the only species to demonstrate an adaptive response to the particular light environment associated with Acer platanoides invasion as predicted by optimal partitioning theory. The profound change in light quantity associated with Acer platanoides canopies appears to act as an important driver of native suppression and conspecific success in invaded riparian communities. Further research is necessary to determine whether the effect of nonnative plant-driven changes on light quantity and quality is a widespread mechanism negatively affecting resident species and facilitating invasion by nonnatives.

Soil Aggregate Stability and Grassland Productivity Associations in a Northern Mixed-Grass Prairie.

Soil aggregate stability data are often predicted to be positively associated with measures of plant productivity, rangeland health, and ecosystem functioning. Here we revisit the hypothesis that soil aggregate stability is positively associated with plant productivity. We measured local (plot-to-plot) variation in grassland community composition, plant (aboveground) biomass, root biomass, % water-stable soil aggregates, and topography. After accounting for spatial autocorrelation, we observed a negative association between % water-stable soil aggregates (0.25-1 and 1-2 mm size classes of macroaggregates) and dominant graminoid biomass, and negative associations between the % water-stable aggregates and the root biomass of a dominant sedge (Carex filifolia). However, variation in total root biomass (0-10 or 0-30 cm depths) was either negatively or not appreciably associated with soil aggregate stabilities. Overall, regression slope coefficients were consistently negative thereby indicating the general absence of a positive association between measures of plant productivity and soil aggregate stability for the study area. The predicted positive association between factors was likely confounded by variation in plant species composition. Specifically, sampling spanned a local gradient in plant community composition which was likely driven by niche partitioning along a subtle gradient in elevation. Our results suggest an apparent trade-off between some measures of plant biomass production and soil aggregate stability, both known to affect the land's capacity to resist erosion. These findings further highlight the uncertainty of plant biomass-soil stability associations.

Epiphyte host preferences and host traits: mechanisms for species-specific interactions.

We investigated species-specific relationships among two species of vascular epiphytes and ten host tree species in a coastal plain forest in the southeastern United States. The epiphytes Tillandsia usneoides and Polypodium polypodioides were highly associated with particular host species in the field, but host traits that favored colonization were inadequate to fully explain the epiphyte-host associations for either epiphyte. Field transplant experiments that bypassed epiphyte colonization demonstrated that the growth of epiphytes was significantly higher on host tree species that naturally bore high epiphyte loads than on host species with few or no epiphytes. These species-specific relationships were highly correlated with the water-holding capacity of the host tree's bark. Positive and negative effects of throughfall, light attenuation by the canopy, and bark stability did not explain the overall patterns of host specificity, but did correlate with some epiphyte-host species relationships. The relative importance of particular host traits differed between the "atmospheric epiphyte" Tillandsia, and the fern Polypodium, which roots in the bark of its hosts. Species-specific interactions among plants, such as those described here, suggest that communities are more than individualistic assemblages of co-occurring species.