The influence of range‐wide plant genetic variation on soil invertebrate communities

Plant genetic variation can have far‐reaching effects on associated communities and ecosystems. Heritable variation in ecologically relevant plant traits is often non‐randomly distributed across a species’ range and can exhibit geographic clines. In the event of range expansions and migration, previously unfamiliar genotypes may have large impacts on resident communities and ecosystems due to the introduction of novel and heritable phenotypic variation. Here we test the hypothesis that geographic origin of a focal plant genotype has effects on belowground invertebrate communities using a common garden field experiment. We sampled soil invertebrates from 103 Oenothera biennis genotypes, which were collected from across the species’ range and planted into a common garden field experiment at the northern range limit. We enumerated 24 000 individuals from 190 morphospecies and found that the diversity, abundance, and composition of soil invertebrate communities varied greatly among plant genotypes. Despite strong effects of plant genotype, we found few genetic correlations between plant traits and soil invertebrate community variables. However, herbivore damage was strongly related to variation in the soil invertebrate community. Geographic origin of plant genotypes had at most a weak effect on belowground communities. We speculate that predicting the extended effects of population movement on associated communities will require detailed knowledge of the trait variation occurring within focal species across particular environmental gradients.     

Genetic mosaics of ecosystem functioning across aspen-dominated landscapes

Genetic diversity is the foundation of all biodiversity, and the genetic variation within species is increasingly recognized as being important to ecosystem level processes. Recent research demonstrates that plant genotype influences above- and belowground communities as well as basic ecosystem functions. However, the extent to which plant genotypes create spatial mosaics of genetically mediated ecosystem processes in natural forests is uncertain. We use Populus tremuloides as a model system to demonstrate the importance of plant genotype on carbon and nitrogen cycling in natural systems. We identified 24 distinct P. tremuloides clones with multiple ramets across 25 km² in southern Wisconsin, United States, using microsatellite makers. We then sampled clone leaf chemistry and belowground nutrient content and microbial extracellular enzyme activity. Aspen-induced variation in belowground carbon and nitrogen content, and microbial activity, varied widely among clones. Variation in green leaf chemistry and belowground microbial activity were correlated with genetic distance among clones, such that more genetically distant clones created more divergent patches of ecosystem processes. These data suggest that aspen genotypes create spatial mosaics of genetically mediated ecosystem functioning across natural landscapes and can therefore have evolutionary consequences for co-occurring species.     

Successional and seasonal variations in soil and litter microbial community structure and function during tropical postagricultural forest regeneration: a multiyear study

Soil microorganisms regulate fundamental biochemical processes in plant litter decomposition and soil organic matter (SOM) transformations. Understanding how microbial communities respond to changes in vegetation is critical for improving predictions of how land‐cover change affects belowground carbon storage and nutrient availability. We measured intra‐ and interannual variability in soil and forest litter microbial community composition and activity via phospholipid fatty acid analysis (PLFA) and extracellular enzyme activity across a well‐replicated, long‐term chronosequence of secondary forests growing on abandoned pastures in the wet subtropical forest life zone of Puerto Rico. Microbial community PLFA structure differed between young secondary forests and older secondary and primary forests, following successional shifts in tree species composition. These successional patterns held across seasons, but the microbial groups driving these patterns differed over time. Microbial community composition from the forest litter differed greatly from those in the soil, but did not show the same successional trends. Extracellular enzyme activity did not differ with forest succession, but varied by season with greater rates of potential activity in the dry seasons. We found few robust significant relationships among microbial community parameters and soil pH, moisture, carbon, and nitrogen concentrations. Observed inter‐ and intrannual variability in microbial community structure and activity reveal the importance of a multiple, temporal sampling strategy when investigating microbial community dynamics with land‐use change. Successional control over microbial composition with forest recovery suggests strong links between above and belowground communities.     

Differential responses of soil bacteria,fungi, archaea and protists to plant species richness and plant functional group identity

Plants are known to influence belowground microbial community structure along their roots, but the impacts of plant species richness and plant functional group (FG) identity on microbial communities in the bulk soil are still not well understood. Here, we used 454‐pyrosequencing to analyse the soil microbial community composition in a long‐term biodiversity experiment at Jena, Germany. We examined responses of bacteria, fungi, archaea, and protists to plant species richness (communities varying from 1 to 60 sown species) and plant FG identity (grasses, legumes, small herbs, tall herbs) in bulk soil. We hypothesized that plant species richness and FG identity would alter microbial community composition and have a positive impact on microbial species richness. Plant species richness had a marginal positive effect on the richness of fungi, but we observed no such effect on bacteria, archaea and protists. Plant species richness also did not have a large impact on microbial community composition. Rather, abiotic soil properties partially explained the community composition of bacteria, fungi, arbuscular mycorrhizal fungi (AMF), archaea and protists. Plant FG richness did not impact microbial community composition; however, plant FG identity was more effective. Bacterial richness was highest in legume plots and lowest in small herb plots, and AMF and archaeal community composition in legume plant communities was distinct from that in communities composed of other plant FGs. We conclude that soil microbial community composition in bulk soil is influenced more by changes in plant FG composition and abiotic soil properties, than by changes in plant species richness per se.     

Punching above their weight: low-biomass non-native plant species alter soil properties during primary succession

Non‐native invasive plants can greatly alter community and ecosystem properties, but efforts to predict which invasive species have the greatest impacts on these properties have been generally unsuccessful. An hypothesis that has considerable promise for predicting the effects of invasive non‐native plant species is the mass ratio hypothesis (i.e. that dominant species exert the strongest effects). We tested this hypothesis using data from a four year removal experiment in which the presence of two dominant shrub species (one native and the other not), and subordinate plant species, were manipulated in factorial combinations over four years in a primary successional floodplain system. We measured the effects of these manipulations on the plant community, soil nutrient status and soil biota in different trophic levels of the soil food web. Our experiment showed that after four years, low‐biomass non‐native plant species exerted disproportionate belowground effects relative to their contribution to total biomass in the plant community, most notably by increasing soil C, soil microbial biomass, altering soil microbial community structure and increasing the abundance of microbial‐feeding and predatory nematodes. Low‐biomass, non‐native plant species had distinct life history strategies and foliar traits (higher foliar N concentrations and higher leaf area per unit mass) compared with the two dominant shrub species (97% of total plant mass). Our results have several implications for understanding species’ effects in communities and on soil properties. First, high‐biomass species do not necessarily exert the largest impacts on community or soil properties. Second, low‐biomass, inconspicuous non‐native species can influence community composition and have important trophic consequences belowground through effects on soil nutrient status or resource availability to soil biota. Our finding that low‐biomass non‐native species influence belowground community structure and soil properties more profoundly than dominant species demonstrates that the mass ratio hypothesis does not accurately predict the relative effects of different coexisting species on community‐ and ecosystem‐level properties.     

Do invasive plants structure microbial communities to accelerate decomposition in intermountain grasslands?

Invasive plants are often associated with greater productivity and soil nutrient availabilities, but whether invasive plants with dissimilar traits change decomposer communities and decomposition rates in consistent ways is little known. We compared decomposition rates and the fungal and bacterial communities associated with the litter of three problematic invaders in intermountain grasslands; cheatgrass (Bromus tectorum), spotted knapweed (Centaurea stoebe) and leafy spurge (Euphorbia esula), as well as the native bluebunch wheatgrass (Pseudoroegneria spicata). Shoot and root litter from each plant was placed in cheatgrass, spotted knapweed, and leafy spurge invasions as well as remnant native communities in a fully reciprocal design for 6 months to see whether decomposer communities were species‐specific, and whether litter decomposed fastest when placed in a community composed of its own species (referred to hereafter as home‐field advantage–HFA). Overall, litter from the two invasive forbs, spotted knapweed and leafy spurge, decomposed faster than the native and invasive grasses, regardless of the plant community of incubation. Thus, we found no evidence of HFA. T‐RFLP profiles indicated that both fungal and bacterial communities differed between roots and shoots and among plant species, and that fungal communities also differed among plant community types. Synthesis. These results show that litter from three common invaders to intermountain grasslands decomposes at different rates and cultures microbial communities that are species‐specific, widespread, and persistent through the dramatic shifts in plant communities associated with invasions.     

Plant diversity does not buffer drought effects on early‐stage litter mass loss rates and microbial properties

Human activities are decreasing biodiversity and changing the climate worldwide. Both global change drivers have been shown to affect ecosystem functioning, but they may also act in concert in a non‐additive way. We studied early‐stage litter mass loss rates and soil microbial properties (basal respiration and microbial biomass) during the summer season in response to plant species richness and summer drought in a large grassland biodiversity experiment, the Jena Experiment, Germany. In line with our expectations, decreasing plant diversity and summer drought decreased litter mass loss rates and soil microbial properties. In contrast to our hypotheses, however, this was only true for mass loss of standard litter (wheat straw) used in all plots, and not for plant community‐specific litter mass loss. We found no interactive effects between global change drivers, that is, drought reduced litter mass loss rates and soil microbial properties irrespective of plant diversity. High mass loss rates of plant community‐specific litter and low responsiveness to drought relative to the standard litter indicate that soil microbial communities were adapted to decomposing community‐specific plant litter material including lower susceptibility to dry conditions during summer months. Moreover, higher microbial enzymatic diversity at high plant diversity may have caused elevated mass loss of standard litter. Our results indicate that plant diversity loss and summer drought independently impede soil processes. However, soil decomposer communities may be highly adapted to decomposing plant community‐specific litter material, even in situations of environmental stress. Results of standard litter mass loss moreover suggest that decomposer communities under diverse plant communities are able to cope with a greater variety of plant inputs possibly making them less responsive to biotic changes.     

Relating belowground microbial composition to the taxonomic,phylogenetic, and functional trait distributions of trees in a tropical forest

The complexities of the relationships between plant and soil microbial communities remain unresolved. We determined the associations between plant aboveground and belowground (root) distributions and the communities of soil fungi and bacteria found across a diverse tropical forest plot. Soil microbial community composition was correlated with the taxonomic and phylogenetic structure of the aboveground plant assemblages even after controlling for differences in soil characteristics, but these relationships were stronger for fungi than for bacteria. In contrast to expectations, the species composition of roots in our soil core samples was a poor predictor of microbial community composition perhaps due to the patchy, ephemeral, and highly overlapping nature of fine root distributions. Our ability to predict soil microbial composition was not improved by incorporating information on plant functional traits suggesting that the most commonly measured plant traits are not particularly useful for predicting the plot‐level variability in belowground microbial communities.     

Soil and plant factors driving the community of soil-borne microorganisms across chronosequences of secondary succession of chalk grasslands with a neutral pH

Although soil pH has been shown to be an important factor driving microbial communities, relatively little is known about the other potentially important factors that shape soil-borne microbial community structure. This study examined plant and microbial communities across a series of neutral pH fields (pH=7.0-7.5) representing a chronosequence of secondary succession after former arable fields were taken out of production. These fields ranged from 17 to >66 years since the time of abandonment, and an adjacent arable field was included as a reference. Hierarchical clustering analysis, nonmetric multidimensional scaling and analysis of similarity of 52 different plant species showed that the plant community composition was significantly different in the different chronosequences, and that plant species richness and diversity increased with time since abandonment. The microbial community structure, as analyzed by phylogenetic microarrays (PhyloChips), was significantly different in arable field and the early succession stage, but no distinct microbial communities were observed for the intermediate and the late succession stages. The most determinant factors in shaping the soil-borne microbial communities were phosphorous and NH(4)(+). Plant community composition and diversity did not have a significant effect on the belowground microbial community structure or diversity.     

Plant Communities, Soil Microorganisms, and Soil Carbon Cycling: Does Altering the World Belowground Matter to Ecosystem Functioning?

Soil microorganisms mediate many critical ecosystem processes. Little is known, however, about the factors that determine soil microbial community composition, and whether microbial community composition influences process rates. Here, we investigated whether aboveground plant diversity affects soil microbial community composition, and whether differences in microbial communities in turn affect ecosystem process rates. Using an experimental system at La Selva Biological Station, Costa Rica, we found that plant diversity (plots contained 1, 3, 5, or > 25 plant species) had a significant effect on microbial community composition (as determined by phospholipid fatty acid analysis). The different microbial communities had significantly different respiration responses to 24 labile carbon compounds. We then tested whether these differences in microbial composition and catabolic capabilities were indicative of the ability of distinct microbial communities to decompose different types of litter in a fully factorial laboratory litter transplant experiment. Both microbial biomass and microbial community composition appeared to play a role in litter decomposition rates. Our work suggests, however, that the more important mechanism through which changes in plant diversity affect soil microbial communities and their carbon cycling activities may be through alterations in their abundance rather than their community composition.     

Legacy of prior host and soil selection on rhizobial fitness in planta

Measuring selection acting on microbial populations in natural or even seminatural environments is challenging because many microbial populations experience variable selection. The majority of rhizobial bacteria are found in the soil. However, they also live symbiotically inside nodules of legume hosts and each nodule can release thousands of daughter cells back into the soil. We tested how past selection (i.e., legacies) by two plant genotypes and by the soil alone affected selection and genetic diversity within a population of 101 strains of Ensifer meliloti. We also identified allelic variants most strongly associated with soil‐ and host‐dependent fitness. In addition to imposing direct selection on rhizobia populations, soil and host environments had lasting effects across host generations. Host presence and genotype during the legacy period explained 22% and 12% of the variance in the strain composition of nodule communities in the second cohort, respectively. Although strains with high host fitness in the legacy cohort tended to be enriched in the second cohort, the diversity of the strain community was greater when the second cohort was preceded by host rather than soil legacies. Our results indicate the potential importance of soil selection driving the evolution of these plant‐associated microbes.     

Intraspecific and intergenerational differences in plant–soil feedbacks

Interactions between plant and soil communities are known to play an integral role in shaping ecosystems. Plants influence the composition of soil communities and soil communities in turn influence plant performance. Such a plant–soil feedback may incur selection pressure on plants and the associating soil community. However, the evolutionary consequences of these above–belowground feedback interactions remain largely speculative. Here we assess whether plant–soil feedback effects differ between intraspecific plant populations and between generations within the same plant population. We used two populations of Trifolium pratense and assessed their performance when grown in association with their home versus away soil biota. Both populations were colonized by distinct microbial communities and performed better with their own home soil communities than with the soil community from the other intraspecific population, demonstrating intraspecific positive feedback effects of home soil. In one of the two populations, we found that plant performance and the root associated microbiota community differed between parental and progeny plants when inoculated with their own home soil. Differences in root associated community characteristics could explain more than 80% of the variation in performance among the progeny and parental plants. Our results highlight that intraspecific differences in both plant and associated soil communities shape plant–soil feedback effects, and consequently indicate that plant–soil feedback can influence the direction of selection between intraspecific plant populations.     

Plant invasion alters nitrogen cycling by modifying the soil nitrifying community

Plant invasions have dramatic aboveground effects on plant community composition, but their belowground effects remain largely uncharacterized. Soil microorganisms directly interact with plants and mediate many nutrient transformations in soil. We hypothesized that belowground changes to the soil microbial community provide a mechanistic link between exotic plant invasion and changes to ecosystem nutrient cycling. To examine this possible link, monocultures and mixtures of exotic and native species were maintained for 4 years in a California grassland. Gross rates of nitrogen (N) mineralization and nitrification were quantified with ¹⁵N pool dilution and soil microbial communities were characterized with DNA‐based methods. Exotic grasses doubled gross nitrification rates, in part by increasing the abundance and changing the composition of ammonia‐oxidizing bacteria in soil. These changes may translate into altered ecosystem N budgets after invasion. Altered soil microbial communities and their resulting effects on ecosystem processes may be an invisible legacy of exotic plant invasions.     

Abiotic drivers and plant traits explain landscape‐scale patterns in soil microbial communities

The controls on aboveground community composition and diversity have been extensively studied, but our understanding of the drivers of belowground microbial communities is relatively lacking, despite their importance for ecosystem functioning. In this study, we fitted statistical models to explain landscape‐scale variation in soil microbial community composition using data from 180 sites covering a broad range of grassland types, soil and climatic conditions in England. We found that variation in soil microbial communities was explained by abiotic factors like climate, pH and soil properties. Biotic factors, namely community‐weighted means (CWM) of plant functional traits, also explained variation in soil microbial communities. In particular, more bacterial‐dominated microbial communities were associated with exploitative plant traits versus fungal‐dominated communities with resource‐conservative traits, showing that plant functional traits and soil microbial communities are closely related at the landscape scale.     

Plants actively control nitrogen cycling: uncorking the microbial bottleneck

Ecologists have tried to link plant species composition and ecosystem properties since the inception of the ecosystem concept in ecology. Many have observed that biological communities could feed back to, and not simply result from, soil properties. But which group of organisms, plants or microorganisms, drive those feedback systems? Recent research asserts that soil microorganisms preclude plant species feedback to soil nitrogen (N) transformations due to strong microbial control of soil N cycling. It has been well documented that litter properties influence soil N cycling. In this review, we stress that under many circumstances plant species exert a major influence over soil N cycling rates via unique N attainment strategies, thus influencing soil N availability and their own fitness. We offer two testable mechanisms by which plants impart active control on the N cycle and thereby allow for plant-litter-soil-plant feedback. Finally, we describe the characteristics of plants and ecosystems that are most likely to exhibit feedback.     

Cascading effects of belowground predators on plant communities are density‐dependent

Soil food webs comprise a multitude of trophic interactions that can affect the composition and productivity of plant communities. Belowground predators feeding on microbial grazers like Collembola could decelerate nutrient mineralization by reducing microbial turnover in the soil, which in turn could negatively influence plant growth. However, empirical evidences for the ecological significance of belowground predators on nutrient cycling and plant communities are scarce. Here, we manipulated predator density (Hypoaspis aculeifer: predatory mite) with equal densities of three Collembola species as a prey in four functionally dissimilar plant communities in experimental microcosms: grass monoculture (Poa pratensis), herb monoculture (Rumex acetosa), legume monoculture (Trifolium pratense), and all three species as a mixed plant community. Density manipulation of predators allowed us to test for density‐mediated effects of belowground predators on Collembola and lower trophic groups. We hypothesized that predator density will reduce Collembola population causing a decrease in nutrient mineralization and hence detrimentally affect plant growth. First, we found a density‐dependent population change in predators, that is, an increase in low‐density treatments, but a decrease in high‐density treatments. Second, prey suppression was lower at high predator density, which caused a shift in the soil microbial community by increasing the fungal: bacterial biomass ratio, and an increase of nitrification rates, particularly in legume monocultures. Despite the increase in nutrient mineralization, legume monocultures performed worse at high predator density. Further, individual grass shoot biomass decreased in monocultures, while it increased in mixed plant communities with increasing predator density, which coincided with elevated soil N uptake by grasses. As a consequence, high predator density significantly increased plant complementarity effects indicating a decrease in interspecific plant competition. These results highlight that belowground predators can relax interspecific plant competition by increasing nutrient mineralization through their density‐dependent cascading effects on detritivore and soil microbial communities.     

Litter and soil biodiversity jointly drive ecosystem functions

The decomposition of litter and the supply of nutrients into and from the soil are two fundamental processes through which the above- and belowground world interact. Microbial biodiversity, and especially that of decomposers, plays a key role in these processes by helping litter decomposition. Yet the relative contribution of litter diversity and soil biodiversity in supporting multiple ecosystem services remains virtually unknown. Here we conducted a mesocosm experiment where leaf litter and soil biodiversity were manipulated to investigate their influence on plant productivity, litter decomposition, soil respiration, and enzymatic activity in the littersphere. We showed that both leaf litter diversity and soil microbial diversity (richness and community composition) independently contributed to explain multiple ecosystem functions. Fungal saprobes community composition was especially important for supporting ecosystem multifunctionality (EMF), plant production, litter decomposition, and activity of soil phosphatase when compared with bacteria or other fungal functional groups and litter species richness. Moreover, leaf litter diversity and soil microbial diversity exerted previously undescribed and significantly interactive effects on EMF and multiple individual ecosystem functions, such as litter decomposition and plant production. Together, our work provides experimental evidence supporting the independent and interactive roles of litter and belowground soil biodiversity to maintain ecosystem functions and multiple services.     

Feedbacks of plant identity and diversity on the diversity and community composition of rhizosphere microbiomes from a long‐term biodiversity experiment

Soil microbes are known to be key drivers of several essential ecosystem processes such as nutrient cycling, plant productivity and the maintenance of plant species diversity. However, how plant species diversity and identity affect soil microbial diversity and community composition in the rhizosphere is largely unknown. We tested whether, over the course of 11 years, distinct soil bacterial communities developed under plant monocultures and mixtures, and if over this time frame plants with a monoculture or mixture history changed in the bacterial communities they associated with. For eight species, we grew offspring of plants that had been grown for 11 years in the same field monocultures or mixtures (plant history in monoculture vs. mixture) in pots inoculated with microbes extracted from the field monoculture and mixture soils attached to the roots of the host plants (soil legacy). After 5 months of growth in the glasshouse, we collected rhizosphere soil from each plant and used 16S rRNA gene sequencing to determine the community composition and diversity of the bacterial communities. Bacterial community structure in the plant rhizosphere was primarily determined by soil legacy and by plant species identity, but not by plant history. In seven of the eight plant species the number of individual operational taxonomic units with increased abundance was larger when inoculated with microbes from mixture soil. We conclude that plant species richness can affect below‐ground community composition and diversity, feeding back to the assemblage of rhizosphere bacterial communities in newly establishing plants via the legacy in soil.     

Soil microbes alter plant fitness under competition and drought

Plants exist across varying biotic and abiotic environments, including variation in the composition of soil microbial communities. The ecological effects of soil microbes on plant communities are well known, whereas less is known about their importance for plant evolutionary processes. In particular, the net effects of soil microbes on plant fitness may vary across environmental contexts and among plant genotypes, setting the stage for microbially mediated plant evolution. Here, we assess the effects of soil microbes on plant fitness and natural selection on flowering time in different environments. We performed two experiments in which we grew Arabidopsis thaliana genotypes replicated in either live or sterilized soil microbial treatments, and across varying levels of either competition (isolation, intraspecific competition or interspecific competition) or watering (well‐watered or drought). We found large effects of competition and watering on plant fitness as well as the expression and natural selection of flowering time. Soil microbes increased average plant fitness under interspecific competition and drought and shaped the response of individual plant genotypes to drought. Finally, plant tolerance to either competition or drought was uncorrelated between soil microbial treatments suggesting that the plant traits favoured under environmental stress may depend on the presence of soil microbes. In summary, our experiments demonstrate that soil microbes can have large effects on plant fitness, which depend on both the environment and individual plant genotype. Future work in natural systems is needed for a complete understanding of the evolutionary importance of interactions between plants and soil microorganisms.     

A shared coevolutionary history does not alter the outcome of coalescence in experimental populations of Pseudomonas fluorescens

Community coalescence, the mixing of multiple communities, is ubiquitous in natural microbial communities. During coalescence, theory suggests the success of a population will be enhanced by the presence of species it has coevolved with (relative to foreign species), because coevolution will result in greater resource specialization to minimize competition. Thus, more coevolved communities should dominate over less coevolved communities during coalescence events. We test these hypotheses using the bacterium Pseudomonas fluorescens which diversifies into coexisting niche‐specialist morphotypes. We first evolved replicate populations for ~40 generations and then isolated evolved genotypes. In a series of competition trials, we determined if using coevolved versus random genotypes affected the relative performance of “communities” of single and multiple genotypes. We found no effect of coevolutionary history on either genotype fitness or community performance, which suggests parallel (co)evolution between communities. However, fitness was enhanced by the presence of other genotypes of the same strain type (wild‐type or an isogenic strain with a LacZ marker; the inclusion of the latter necessary to distinguish genotypes during competition), indicative of local adaptation with respect to genetic background. Our results are the first to investigate the effect of (co)evolution on the outcome of coalescence and suggest that when input populations are functionally similar and added at equal mixing ratios, the outcome community may not be asymmetrically dominated by either input population.