Soil legacy effects of plants and drought on aboveground insects in native and range-expanding plant communities.

Soils contain biotic and abiotic legacies of previous conditions that may influence plant community biomass and associated aboveground biodiversity. However, little is known about the relative strengths and interactions of the various belowground legacies on aboveground plant-insect interactions. We used an outdoor mesocosm experiment to investigate the belowground legacy effects of range-expanding versus native plants, extreme drought and their interactions on plants, aphids and pollinators. We show that plant biomass was influenced more strongly by the previous plant community than by the previous summer drought. Plant communities consisted of four congeneric pairs of natives and range expanders, and their responses were not unanimous. Legacy effects affected the abundance of aphids more strongly than pollinators. We conclude that legacies can be contained as soil 'memories' that influence aboveground plant community interactions in the next growing season. These soil-borne 'memories' can be altered by climate warming-induced plant range shifts and extreme drought.

Linking changes in species composition and biomass in a globally distributed grassland experiment.

Global change drivers, such as anthropogenic nutrient inputs, are increasing globally. Nutrient deposition simultaneously alters plant biodiversity, species composition and ecosystem processes like aboveground biomass production. These changes are underpinned by species extinction, colonisation and shifting relative abundance. Here, we use the Price equation to quantify and link the contributions of species that are lost, gained or that persist to change in aboveground biomass in 59 experimental grassland sites. Under ambient (control) conditions, compositional and biomass turnover was high, and losses (i.e. local extinctions) were balanced by gains (i.e. colonisation). Under fertilisation, the decline in species richness resulted from increased species loss and decreases in species gained. Biomass increase under fertilisation resulted mostly from species that persist and to a lesser extent from species gained. Drivers of ecological change can interact relatively independently with diversity, composition and ecosystem processes and functions such as aboveground biomass due to the individual contributions of species lost, gained or persisting.

Temporal dynamics of range expander and congeneric native plant responses during and after extreme drought events.

Climate change is causing range shifts of many species to higher latitudes and altitudes and increasing their exposure to extreme weather events. It has been shown that range-shifting plant species may perform differently in new soil than related natives; however, little is known about how extreme weather events affect range-expanding plants compared to related natives. In this study we used outdoor mesocosms to study how range-expanding plant species responded to extreme drought in live soil from a habitat in a new range with and without live soil from a habitat in the original range (Hungary). During summer drought, the shoot biomass of the range-expanding plant community declined. In spite of this, in the mixed community, range expanders produced more shoot biomass than congeneric natives. In mesocosms with a history of range expanders in the previous year, native plants produced less biomass. Plant legacy or soil origin effects did not change the response of natives or range expanders to summer drought. During rewetting, range expanders had less biomass than congeneric natives but higher drought resilience (survival) in soils from the new range where in the previous year native plant species had grown. The biomass patterns of the mixed plant communities were dominated by Centaurea spp.; however, not all plant species within the groups of natives and of range expanders showed the general pattern. Drought reduced the litter decomposition, microbial biomass, and abundances of bacterivorous, fungivorous, and carnivorous nematodes. Their abundances recovered during rewetting. There was less microbial and fungal biomass, and there were fewer fungivorous nematodes in soils from the original range where range expanders had grown in the previous year. We concluded that in mixed plant communities of range expanders and congeneric natives, range expanders performed better, under both ambient and drought conditions, than congeneric natives. However, when considering the responses of individual species, we observed variations among pairs of congenerics, so that under the present mixed-community conditions there was no uniformity in responses to drought of range expanders versus congeneric natives. Range-expanding plant species reduced soil fungal biomass and the numbers of soil fungivorous nematodes, suggesting that the effects of range-expanding plant species can trickle up in the soil food web.

Soil microbial diversity and community composition during conversion from conventional to organic agriculture.

It is generally assumed that the dependence of conventional agriculture on artificial fertilizers and pesticides strongly impacts the environment, while organic agriculture relying more on microbial functioning may mitigate these impacts. However, it is not well known how microbial diversity and community composition change in conventionally managed farmers' fields that are converted to organic management. Here, we sequenced bacterial and fungal communities of 34 organic fields on sand and marine clay soils in a time series (chronosequence) covering 25 years of conversion. Nearby conventional fields were used as references. We found that community composition of bacteria and fungi differed between organic and conventionally managed fields. In the organic fields, fungal diversity increased with time since conversion. However, this effect disappeared when the conventional paired fields were included. There was a relationship between pH and soil organic matter content and the diversity and community composition of bacteria and fungi. In marine clay soils, when time since organic management increased, fungal communities in organic fields became more dissimilar to those in conventional fields. We conclude that conversion to organic management in these Dutch farmers' fields did not increase microbial community diversity. Instead, we observed that in organic fields in marine clay when time since conversion increased soil fungal community composition became progressively dissimilar from that in conventional fields. Our results also showed that the paired sampling approach of organic and conventional fields was essential in order to control for environmental variation that was otherwise unaccounted for.

Home-field advantage of litter decomposition: from the phyllosphere to the soil.

Plants often associate with specialized decomposer communities that increase plant litter breakdown, a phenomenon that is known as the 'home-field advantage' (HFA). Although the concept of HFA has long considered only the role of the soil microbial community, explicit consideration of the role of the microbial community on the foliage before litter fall (i.e. the phyllosphere community) may help us to better understand HFA. We investigated the occurrence of HFA in the presence vs absence of phyllosphere communities and found that HFA effects were smaller when phyllosphere communities were removed. We propose that priority effects and interactions between phyllosphere and soil organisms can help explain the positive effects of the phyllosphere at home, and suggest a path forward for further investigation.

Nutrient availability controls the impact of mammalian herbivores on soil carbon and nitrogen pools in grasslands.

Grasslands are subject to considerable alteration due to human activities globally, including widespread changes in populations and composition of large mammalian herbivores and elevated supply of nutrients. Grassland soils remain important reservoirs of carbon (C) and nitrogen (N). Herbivores may affect both C and N pools and these changes likely interact with increases in soil nutrient availability. Given the scale of grassland soil fluxes, such changes can have striking consequences for atmospheric C concentrations and the climate. Here, we use the Nutrient Network experiment to examine the responses of soil C and N pools to mammalian herbivore exclusion across 22 grasslands, under ambient and elevated nutrient availabilities (fertilized with NPK + micronutrients). We show that the impact of herbivore exclusion on soil C and N pools depends on fertilization. Under ambient nutrient conditions, we observed no effect of herbivore exclusion, but under elevated nutrient supply, pools are smaller upon herbivore exclusion. The highest mean soil C and N pools were found in grazed and fertilized plots. The decrease in soil C and N upon herbivore exclusion in combination with fertilization correlated with a decrease in aboveground plant biomass and microbial activity, indicating a reduced storage of organic matter and microbial residues as soil C and N. The response of soil C and N pools to herbivore exclusion was contingent on temperature - herbivores likely cause losses of C and N in colder sites and increases in warmer sites. Additionally, grasslands that contain mammalian herbivores have the potential to sequester more N under increased temperature variability and nutrient enrichment than ungrazed grasslands. Our study highlights the importance of conserving mammalian herbivore populations in grasslands worldwide. We need to incorporate local-scale herbivory, and its interaction with nutrient enrichment and climate, within global-scale models to better predict land-atmosphere interactions under future climate change.

Biodiversity-ecosystem functioning relationships in a long-term non-weeded field experiment.

Many grassland biodiversity experiments show a positive relationship between biodiversity and ecosystem functioning, however, in most of these experiments plant communities are established by sowing and natural colonization is prevented by selective weeding of non-sown species. During ecosystem restoration, for example on abandoned fields, plant communities start on bare soil, and diversity is often manipulated in a single sowing event. How such initial plant diversity manipulations influence plant biodiversity development and ecosystem functioning is not well understood. We examined how relationships between taxonomic and functional diversity, biomass production and stability develop over 16 yr in non-weeded plots sown with 15 species, four species, or that were not sown. We found that sown plant communities become functionally similar to unsown, naturally colonized plant communities. However, initial sowing treatments had long-lasting effects on species composition and taxonomic diversity. We found only few relationships between biomass production, or stability in biomass production, and functional or taxonomic diversity, and the ones we observed were negative. In addition, the cover of dominant plant species was positively related to biomass production and stability. We conclude that effects of introducing plant species at the start of secondary succession can persist for a long time, and that in secondary succession communities with natural plant species dynamics diversity-functioning relationships can be weak or negative. Moreover, our findings indicate that in systems where natural colonization of species is allowed effects of plant dominance may underlie diversity-functioning relationships.

Effects of root decomposition on plant-soil feedback of early- and mid-successional plant species.

Plant-soil feedback (PSF) is an important driver of plant community dynamics. Many studies have emphasized the role of pathogens and symbiotic mutualists in PSFs; however, less is known about the contribution of decomposing litter, especially that of roots. We conducted a PSF experiment, where soils were conditioned by living early- and mid-successional grasses and forbs with and without decomposing roots of conspecific species (conditioning phase). These soils were used to test growth responses of conspecific and heterospecific plant species (feedback phase). The addition of the roots of conspecifics decreased the biomass of both early- and mid-successional plant species in the conditioning phase. In the feedback phase, root addition had positive effects on the biomass of early-successional species and neutral effects on mid-successional species, except when mid-successional grasses were grown in soils conditioned by conspecifics, where effects were negative. Biomass of early- and mid-successional forbs was generally reduced in soils conditioned by conspecifics. We conclude that root decomposition may increase short-term negative PSF effects, but that the effects can become neutral to positive over time, thereby counteracting negative components of PSF. This implies that root decomposition is a key element of PSF and needs to be included in future studies.

Tree and shrub richness modifies subtropical tree productivity by regulating the diversity and community composition of soil bacteria and archaea.

BACKGROUND: Declines in plant biodiversity often have negative consequences for plant community productivity, and it becomes increasingly acknowledged that this may be driven by shifts in soil microbial communities. So far, the role of fungal communities in driving tree diversity-productivity relationships has been well assessed in forests. However, the role of bacteria and archaea, which are also highly abundant in forest soils and perform pivotal ecosystem functions, has been less investigated in this context. Here, we investigated how tree and shrub richness affects stand-level tree productivity by regulating bacterial and archaeal community diversity and composition. We used a landscape-scale, subtropical tree biodiversity experiment (BEF-China) where tree (1, 2, or 4 species) and shrub richness (0, 2, 4, 8 species) were modified. RESULTS: Our findings indicated a noteworthy decline in soil bacterial α-diversity as tree species richness increased from monoculture to 2- and 4- tree species mixtures, but a significant increase in archaeal α-diversity. Additionally, we observed that the impact of shrub species richness on microbial α-diversity was largely dependent on the level of tree species richness. The increase in tree species richness greatly reduced the variability in bacterial community composition and the complexity of co-occurrence network, but this effect was marginal for archaea. Both tree and shrub species richness increased the stand-level tree productivity by regulating the diversity and composition of bacterial community and archaeal diversity, with the effects being mediated via increases in soil C:N ratios. CONCLUSIONS: Our findings provide insight into the importance of bacterial and archaeal communities in driving the relationship between plant diversity and productivity in subtropical forests and highlight the necessity for a better understanding of prokaryotic communities in forest soils. Video Abstract.

The positive effect of plant diversity on soil carbon depends on climate.

Little is currently known about how climate modulates the relationship between plant diversity and soil organic carbon and the mechanisms involved. Yet, this knowledge is of crucial importance in times of climate change and biodiversity loss. Here, we show that plant diversity is positively correlated with soil carbon content and soil carbon-to-nitrogen ratio across 84 grasslands on six continents that span wide climate gradients. The relationships between plant diversity and soil carbon as well as plant diversity and soil organic matter quality (carbon-to-nitrogen ratio) are particularly strong in warm and arid climates. While plant biomass is positively correlated with soil carbon, plant biomass is not significantly correlated with plant diversity. Our results indicate that plant diversity influences soil carbon storage not via the quantity of organic matter (plant biomass) inputs to soil, but through the quality of organic matter. The study implies that ecosystem management that restores plant diversity likely enhances soil carbon sequestration, particularly in warm and arid climates.

Environmental heterogeneity modulates the effect of plant diversity on the spatial variability of grassland biomass.

Plant productivity varies due to environmental heterogeneity, and theory suggests that plant diversity can reduce this variation. While there is strong evidence of diversity effects on temporal variability of productivity, whether this mechanism extends to variability across space remains elusive. Here we determine the relationship between plant diversity and spatial variability of productivity in 83 grasslands, and quantify the effect of experimentally increased spatial heterogeneity in environmental conditions on this relationship. We found that communities with higher plant species richness (alpha and gamma diversity) have lower spatial variability of productivity as reduced abundance of some species can be compensated for by increased abundance of other species. In contrast, high species dissimilarity among local communities (beta diversity) is positively associated with spatial variability of productivity, suggesting that changes in species composition can scale up to affect productivity. Experimentally increased spatial environmental heterogeneity weakens the effect of plant alpha and gamma diversity, and reveals that beta diversity can simultaneously decrease and increase spatial variability of productivity. Our findings unveil the generality of the diversity-stability theory across space, and suggest that reduced local diversity and biotic homogenization can affect the spatial reliability of key ecosystem functions.

Large grazers modify effects of aboveground-belowground interactions on small-scale plant community composition.

Aboveground and belowground organisms influence plant community composition by local interactions, and their scale of impact may vary from millimeters belowground to kilometers aboveground. However, it still poorly understood how large grazers that select their forage on large spatial scales interact with small-scale aboveground-belowground interactions on plant community heterogeneity. Here, we investigate how cattle (Bos taurus) modify the effects of interactions between yellow meadow ants (Lasius flavus) and European brown hares (Lepus europaeus) on the formation of small-scale heterogeneity in vegetation composition. In the absence of cattle, hares selectively foraged on ant mounds, while under combined grazing by hares and cattle, vertebrate grazing pressure was similar on and off mounds. Ant mounds that were grazed by only hares had a different plant community composition compared to their surroundings: the cover of the grazing-intolerant grass Elytrigia atherica was reduced on ant mounds, whereas the relative cover of the more grazing-tolerant and palatable grass Festuca rubra was enhanced. Combined grazing by hares and cattle, resulted in homogenization of plant community composition on and off ant mounds, with high overall cover of F. rubra. We conclude that hares can respond to local ant-soil-vegetation interactions, because they are small, selective herbivores that make their foraging decisions on a local scale. This results in small-scale plant patches on mounds of yellow meadow ants. In the presence of cattle, which are less selective aboveground herbivores, local plant community patterns triggered by small-scale aboveground-belowground interactions can disappear. Therefore, cattle modify the consequences of aboveground-belowground interactions for small-scale plant community composition.

Microbial storage and its implications for soil ecology.

Organisms throughout the tree of life accumulate chemical resources, in particular forms or compartments, to secure their availability for future use. Here we review microbial storage and its ecological significance by assembling several rich but disconnected lines of research in microbiology, biogeochemistry, and the ecology of macroscopic organisms. Evidence is drawn from various systems, but we pay particular attention to soils, where microorganisms play crucial roles in global element cycles. An assembly of genus-level data demonstrates the likely prevalence of storage traits in soil. We provide a theoretical basis for microbial storage ecology by distinguishing a spectrum of storage strategies ranging from surplus storage (storage of abundant resources that are not immediately required) to reserve storage (storage of limited resources at the cost of other metabolic functions). This distinction highlights that microorganisms can invest in storage at times of surplus and under conditions of scarcity. We then align storage with trait-based microbial life-history strategies, leading to the hypothesis that ruderal species, which are adapted to disturbance, rely less on storage than microorganisms adapted to stress or high competition. We explore the implications of storage for soil biogeochemistry, microbial biomass, and element transformations and present a process-based model of intracellular carbon storage. Our model indicates that storage can mitigate against stoichiometric imbalances, thereby enhancing biomass growth and resource-use efficiency in the face of unbalanced resources. Given the central roles of microbes in biogeochemical cycles, we propose that microbial storage may be influential on macroscopic scales, from carbon cycling to ecosystem stability.

Evolutionary history of grazing and resources determine herbivore exclusion effects on plant diversity.

Ecological models predict that the effects of mammalian herbivore exclusion on plant diversity depend on resource availability and plant exposure to ungulate grazing over evolutionary time. Using an experiment replicated in 57 grasslands on six continents, with contrasting evolutionary history of grazing, we tested how resources (mean annual precipitation and soil nutrients) determine herbivore exclusion effects on plant diversity, richness and evenness. Here we show that at sites with a long history of ungulate grazing, herbivore exclusion reduced plant diversity by reducing both richness and evenness and the responses of richness and diversity to herbivore exclusion decreased with mean annual precipitation. At sites with a short history of grazing, the effects of herbivore exclusion were not related to precipitation but differed for native and exotic plant richness. Thus, plant species' evolutionary history of grazing continues to shape the response of the world's grasslands to changing mammalian herbivory.

Protists as catalyzers of microbial litter breakdown and carbon cycling at different temperature regimes.

Soil bacteria and fungi are key drivers of carbon released from soils to the atmosphere through decomposition of plant-derived organic carbon sources. This process has important consequences for the global climate. While global change factors, such as increased temperature, are known to affect bacterial- and fungal-mediated decomposition rates, the role of trophic interactions in affecting decomposition remains largely unknown. We designed synthetic microbial communities consisting of eight bacterial and eight fungal species and tested the influence of predation by a model protist, Physarum polycephalum, on litter breakdown at 17 and 21 °C. Protists increased CO2 release and litter mass loss by ~35% at 17 °C lower temperatures, while they only had minor effects on microbial-driven CO2 release and mass loss at 21 °C. We found species-specific differences in predator-prey interactions, which may affect microbial community composition and functioning and thus underlie the impact of protists on litter breakdown. Our findings suggest that microbial predation by fast-growing protists is of under-appreciated functional importance, as it affects decomposition and, as such, may influence global carbon dynamics. Our results indicate that we need to better understand the role of trophic interactions within the microbiome in controlling decomposition processes and carbon cycling.

Plant-Soil Feedbacks and Temporal Dynamics of Plant Diversity-Productivity Relationships.

Plant-soil feedback (PSF) and diversity-productivity relationships are important research fields to study drivers and consequences of changes in plant biodiversity. While studies suggest that positive plant diversity-productivity relationships can be explained by variation in PSF in diverse plant communities, key questions on their temporal relationships remain. Here, we discuss three processes that change PSF over time in diverse plant communities, and their effects on temporal dynamics of diversity-productivity relationships: spatial redistribution and changes in dominance of plant species; phenotypic shifts in plant traits; and dilution of soil pathogens and increase in soil mutualists. Disentangling these processes in plant diversity experiments will yield new insights into how plant diversity-productivity relationships change over time.

Belowground community turnover accelerates the decomposition of standing dead wood.

Standing dead trees (snags) decompose more slowly than downed dead wood and provide critical habitat for many species. The rate at which snags fall therefore influences forest carbon dynamics and biodiversity. Fall rates correlate strongly with mean annual temperature, presumably because warmer climates facilitate faster wood decomposition and hence degradation of the structural stability of standing wood. These faster decomposition rates coincide with turnover from fungal-dominated wood decomposer communities in cooler forests to codomination by fungi and termites in warmer regions. A key question for projecting forest dynamics is therefore whether temperature effects on wood decomposition arise primarily because warmer conditions facilitate faster decomposer metabolism, or are also influenced indirectly by belowground community turnover (e.g., termites exert additional influence beyond fungal-plus-bacterial mediated decomposition). To test between these possibilities, we simulate standing dead trees with untreated wooden posts and follow them in the field across 5 yr at 12 sites, before measuring buried, soil-air interface and aerial post sections to quantify wood decomposition and organism activities. High termite activities at the warmer sites are associated with rates of postfall that are three times higher than at the cooler sites. Termites primarily consume buried wood, with decomposition rates greatest where termite activities are highest. However, where higher microbial and termite activities co-occur, they appear to compensate for one another first, and then to slow decomposition rates at their highest activities, suggestive of interference competition. If the range of microbial and termite codomination of wood decomposer communities expands under climate warming, our data suggest that expansion will accelerate snag fall with consequent effects on forest carbon cycling and biodiversity in forests previously dominated by microbial decomposers.

Vertebrate herbivores influence soil nematodes by modifying plant communities.

Abiotic soil properties, plant community composition, and herbivory all have been reported as important factors influencing the composition of soil communities. However, most studies thus far have considered these factors in isolation, whereas they strongly interact in the field. Here, we study how grazing by vertebrate herbivores influences the soil nematode community composition of a floodplain grassland while we account for effects of grazing on plant community composition and abiotic soil properties. Nematodes are the most ubiquitous invertebrates in the soil. They include a variety of feeding types, ranging from microbial feeders to herbivores and carnivores, and they perform key functions in soil food webs. Our hypothesis was that grazing affects nematode community structure and composition through altering plant community structure and composition. Alternatively, we tested whether the effects of grazing may, directly or indirectly, run via changes in soil abiotic properties. We used a long-term field experiment containing plots with and without vertebrate grazers (cattle and rabbits). We compared plant and nematode community structure and composition, as well as a number of key soil abiotic properties, and we applied structural equation modeling to investigate four possible pathways by which grazing may change nematode community composition. Aboveground grazing increased plant species richness and reduced both plant and nematode community heterogeneity. There was a positive relationship between plant and nematode diversity indices. Grazing decreased the number of bacterial-feeding nematodes, indicating that in these grasslands, top-down control of plant production by grazing leads to bottom-up control in the basal part of the bacterial channel of the soil food web. According to the structural equation model, grazing had a strong effect on soil abiotic properties and plant community composition, whereas plant community composition was the main determinant of nematode community composition. Other pathways, which assumed that grazing influenced nematode community composition by inducing changes in soil abiotic properties, did not significantly explain variation in nematode community composition. We conclude that grazing-induced changes in nematode community composition mainly operated via changes in plant community composition. Influences of vertebrate grazers on soil nematodes through modification of abiotic soil properties were of less importance.

The abundance of arbuscular mycorrhiza in soils is linked to the total length of roots colonized at ecosystem level.

Arbuscular mycorrhizal fungi (AMF) strongly affect ecosystem functioning. To understand and quantify the mechanisms of this control, knowledge about the relationship between the actual abundance and community composition of AMF in the soil and in plant roots is needed. We collected soil and root samples in a natural dune grassland to test whether, across a plant community, the abundance of AMF in host roots (measured as the total length of roots colonized) is related to soil AMF abundance (using the neutral lipid fatty acids (NLFA) 16:1ω5 as proxy). Next-generation sequencing was used to explore the role of community composition in abundance patterns. We found a strong positive relationship between the total length of roots colonized by AMF and the amount of NLFA 16:1ω5 in the soil. We provide the first field-based evidence of proportional biomass allocation between intra-and extraradical AMF mycelium, at ecosystem level. We suggest that this phenomenon is made possible by compensatory colonization strategies of individual fungal species. Finally, our findings open the possibility of using AMF total root colonization as a proxy for soil AMF abundances, aiding further exploration of the AMF impacts on ecosystems functioning.