Gerlinde B. De Deyn

Plant functional traits and soil carbon sequestration in contrasting biomes

Plant functional traits control a variety of terrestrial ecosystem processes, including soil carbon storage which is a key component of the global carbon cycle. Plant traits regulate net soil carbon storage by controlling carbon assimilation, its transfer and storage in belowground biomass, and its release from soil through respiration, fire and leaching. However, our mechanistic understanding of these processes is incomplete. Here, we present a mechanistic framework, based on the plant traits that drive soil carbon inputs and outputs, for understanding how alteration of vegetation composition will affect soil carbon sequestration under global changes. First, we show direct and indirect plant trait effects on soil carbon input and output through autotrophs and heterotrophs, and through modification of abiotic conditions, which need to be considered to determine the local carbon sequestration potential. Second, we explore how the composition of key plant traits and soil biota related to carbon input, release and storage prevail in different biomes across the globe, and address the biome-specific mechanisms by which plant trait composition may impact on soil carbon sequestration. We propose that a trait-based approach will help to develop strategies to preserve and promote carbon sequestration.

Soil invertebrate fauna enhances grassland succession and diversity

One of the most important areas in ecology is to elucidate the factors that drive succession in ecosystems and thus influence the diversity of species in natural vegetation. Significant mechanisms in this process are known to be resource limitation and the effects of aboveground vertebrate herbivores. More recently, symbiotic and pathogenic soil microbes have been shown to exert a profound effect on the composition of vegetation and changes therein. However, the influence of invertebrate soil fauna on succession has so far received little attention. Here we report that invertebrate soil fauna might enhance both secondary succession and local plant species diversity. Soil fauna from a series of secondary grassland succession stages selectively suppress early successional dominant plant species, thereby enhancing the relative abundance of subordinate species and also that of species from later succession stages. Soil fauna from the mid-succession stage had the strongest effect. Our results clearly show that soil fauna strongly affects the composition of natural vegetation and we suggest that this knowledge might improve the restoration and conservation of plant species diversity.

Selection for niche differentiation in plant communities increases biodiversity effects

In experimental plant communities, relationships between biodiversity and ecosystem functioning have been found to strengthen over time, a fact often attributed to increased resource complementarity between species in mixtures and negative plant–soil feedbacks in monocultures. Here we show that selection for niche differentiation between species can drive this increasing biodiversity effect. Growing 12 grassland species in test monocultures and mixtures, we found character displacement between species and increased biodiversity effects when plants had been selected over 8 years in species mixtures rather than in monocultures. When grown in mixtures, relative differences in height and specific leaf area between plant species selected in mixtures (mixture types) were greater than between species selected in monocultures (monoculture types). Furthermore, net biodiversity and complementarity effects were greater in mixtures of mixture types than in mixtures of monoculture types. Our study demonstrates a novel mechanism for the increase in biodiversity effects: selection for increased niche differentiation through character displacement. Selection in diverse mixtures may therefore increase species coexistence and ecosystem functioning in natural communities and may also allow increased mixture yields in agriculture or forestry. However, loss of biodiversity and prolonged selection of crops in monoculture may compromise this potential for selection in the longer term.

Plant species richness, identity and productivity differentially influence key groups of microbes in grassland soils of contrasting fertility

The abundance of microbes in soil is thought to be strongly influenced by plant productivity rather than by plant species richness per se. However, whether this holds true for different microbial groups and under different soil conditions is unresolved. We tested how plant species richness, identity and biomass influence the abundances of arbuscular mycorrhizal fungi (AMF), saprophytic bacteria and fungi, and actinomycetes, in model plant communities in soil of low and high fertility using phospholipid fatty acid analysis. Abundances of saprophytic fungi and bacteria were driven by larger plant biomass in high diversity treatments. In contrast, increased AMF abundance with larger plant species richness was not explained by plant biomass, but responded to plant species identity and was stimulated by Anthoxantum odoratum. Our results indicate that the abundance of saprophytic soil microbes is influenced more by resource quantity, as driven by plant production, while AMF respond more strongly to resource composition, driven by variation in plant species richness and identity. This suggests that AMF abundance in soil is more sensitive to changes in plant species diversity per se and plant species composition than are abundances of saprophytic microbes.

Plant species richness promotes soil carbon and nitrogen stocks in grasslands without legumes

Summary 1. The storage of carbon (C) and nitrogen (N) in soil is important ecosystem functions. Grassland biodiversity experiments have shown a positive effect of plant diversity on soil C and N storage. However, these experiments all included legumes, which constitute an important N input through N2-fixation. Indeed, the results of these experiments suggest that N2 fixation by legumes is a major driver of soil C and N storage. 2. We studied whether plant diversity affects soil C and N storage in the absence of legumes. In an 11-year grassland biodiversity experiment without legumes, we measured soil C and N stocks. We further determined above-ground biomass productivity, standing root biomass, soil organic matter decomposition and N mineralization rates to understand the mechanisms underlying the change in soil C and N stocks in relation to plant diversity and their feedbacks to plant productivity. 3. We found that soil C and N stocks increased by 18% and 16% in eight-species mixtures compared to the average of monocultures of the same species, respectively. Increased soil C and N stocks were mainly driven by increased C input and N retention, resulting from enhanced plant productivity, which surpassed enhanced C loss from decomposition. Importantly, higher soil C and N stocks were associated with enhanced soil N mineralization rates, which can explain the strengthening of the positive diversity–productivity relationship observed in the last years of the experiment. 4. Synthesis. We demonstrated that also in the absence of legumes, plant species richness promotes soil carbon (C) and nitrogen (N) stocks via increased plant productivity. In turn, enhanced soil C and N stocks showed a positive feedback to plant productivity via enhanced N mineralization, which could further accelerate soil C and N storage in the long term.

Soil biotic legacy effects of extreme weather events influence plant invasiveness

Climate change is expected to increase future abiotic stresses on ecosystems through extreme weather events leading to more extreme drought and rainfall incidences [Jentsch A, et al. (2007) Front Ecol Environ 5(7):365–374]. These fluctuations in precipitation may affect soil biota, soil processes [Evans ST, Wallenstein MD (2012) Biogeochemistry 109:101–116], and the proportion of exotics in invaded plant communities [Jiménez MA, et al. (2011) Ecol Lett 14:1277–1235]. However, little is known about legacy effects in soil on the performance of exotics and natives in invaded plant communities. Here we report that drought and rainfall effects on soil processes and biota affect the performance of exotics and natives in plant communities. We performed two mesocosm experiments. In the first experiment, soil without plants was exposed to drought and/or rainfall, which affected soil N availability. Then the initial soil moisture conditions were restored, and a mixed community of co-occurring natives and exotics was planted and exposed to drought during growth. A single stress before or during growth decreased the biomass of natives, but did not affect exotics. A second drought stress during plant growth resetted the exotic advantage, whereas native biomass was not further reduced. In the second experiment, soil inoculation revealed that drought and/or rainfall influenced soil biotic legacies, which promoted exotics but suppressed natives. Our results demonstrate that extreme weather events can cause legacy effects in soil biota, promoting exotics and suppressing natives in invaded plant communities, depending on the type, frequency, and timing of extreme events.

Chemical defense, mycorrhizal colonization and growth responses in Plantago lanceolata L.

Allelochemicals defend plants against herbivore and pathogen attack aboveground and belowground. Whether such plant defenses incur ecological costs by reducing benefits from plant mutualistic symbionts is largely unknown. We explored a potential trade-off between inherent plant chemical defense and belowground mutualism with arbuscular mycorrhizal fungi (AMF) in Plantago lanceolata L., using plant genotypes from lines selected for low and high constitutive levels of the iridoid glycosides (IG) aucubin and catalpol. As selection was based on IG concentrations in leaves, we first examined whether IG concentrations covaried in roots. Root and leaf IG concentrations were strongly positively correlated among genotypes, indicating genetic interdependence of leaf and root defense. We then found that root AMF arbuscule colonization was negatively correlated with root aucubin concentration. This negative correlation was observed both in plants grown with monocultures of Glomus intraradices and in plants colonized from whole-field soil inoculum. Overall, AMF did not affect total biomass of plants; an enhancement of initial shoot biomass was offset by a lower root biomass and reduced regrowth after defoliation. Although the precise effects of AMF on plant biomass varied among genotypes, plants with high IG levels and low AMF arbuscule colonization in roots did not produce less biomass than plants with low IG and high AMF arbuscule colonization. Therefore, although an apparent trade-off was observed between high root chemical defense and AMF arbuscule colonization, this did not negatively affect the growth responses of the plants to AMF. Interestingly, AMF induced an increase in root aucubin concentration in the high root IG genotype of P. lanceolata. We conclude that AMF does not necessarily stimulate plant growth, that direct plant defense by secondary metabolites does not necessarily reduce potential benefits from AMF, and that AMF can enhance concentrations of root chemical defenses, but that these responses are plant genotype-dependent.

Plant species identity surpasses species richness as a key driver of N2O emissions from grassland

Grassland ecosystems worldwide not only provide many important ecosystem services but they also function as a major source of the greenhouse gas nitrous oxide (N2O), especially in response to nitrogen deposition by grazing animals. To explore the role of plants as mediators of these emissions, we tested whether and how N2O emissions are dependent on grass species richness and/or specific grass species composition in the absence and presence of urine deposition. We hypothesized that: (i) N2O emissions relate negatively to plant productivity; (ii) four-species mixtures have lower emissions than monocultures (as they are expected to be more productive); (iii) emissions are lowest in combinations of species with diverging root morphology and high root biomass; and (iv) the identity of the key species that reduce N2O emissions is dependent on urine deposition. We established monocultures and two- and four-species mixtures of common grass species with diverging functional traits: Lolium perenne L. (Lp), Festuca arundinacea Schreb. (Fa), Phleum pratense L. (Php) and Poa trivialis L. (Pt), and quantified N2O emissions for 42 days. We found no relation between plant species richness and N2O emissions. However, N2O emissions were significantly reduced in specific plant species combinations. In the absence of urine, plant communities of Fa+Php acted as a sink for N2O, whereas the monocultures of these species constituted a N2O source. With urine application Lp+Pt plant communities reduced (P < 0.001) N2O emissions by 44% compared to monocultures of Lp. Reductions in N2O emissions by species mixtures could be explained by total biomass productivity and by complementarity in root morphology. This study shows that plant species composition is a key component underlying N2O emissions from grassland ecosystems. Selection of specific grass species combinations in the context of the expected nitrogen deposition regimes may therefore provide a key for mitigation of N2O emissions.

Plant diversity and root traits benefit physical properties key to soil function in grasslands

Abstract Plant diversity loss impairs ecosystem functioning, including important effects on soil. Most studies that have explored plant diversity effects belowground, however, have largely focused on biological processes. As such, our understanding of how plant diversity impacts the soil physical environment remains limited, despite the fundamental role soil physical structure plays in ensuring soil function and ecosystem service provision. Here, in both a glasshouse and a long‐term field study, we show that high plant diversity in grassland systems increases soil aggregate stability, a vital structural property of soil, and that root traits play a major role in determining diversity effects. We also reveal that the presence of particular plant species within mixed communities affects an even wider range of soil physical processes, including hydrology and soil strength regimes. Our results indicate that alongside well‐documented effects on ecosystem functioning, plant diversity and root traits also benefit essential soil physical properties.

Soil invertebrate fauna affect N2O emissions from soil

Nitrous oxide (N2 O) emissions from soils contribute significantly to global warming. Mitigation of N2 O emissions is severely hampered by a lack of understanding of its main controls. Fluxes can only partly be predicted from soil abiotic factors and microbial analyses - a possible role for soil fauna has until now largely been overlooked. We studied the effect of six groups of soil invertebrate fauna and tested the hypothesis that all of them increase N2 O emissions, although to different extents. We conducted three microcosm experiments with sandy soil and hay residue. Faunal groups included in our experiments were as follows: fungal-feeding nematodes, mites, springtails, potworms, earthworms and isopods. In experiment I, involving all six faunal groups, N2 O emissions declined with earthworms and potworms from 78.4 (control) to 37.0 (earthworms) or 53.5 (potworms) mg N2 O-N m(-2) . In experiment II, with a higher soil-to-hay ratio and mites, springtails and potworms as faunal treatments, N2 O emissions increased with potworms from 51.9 (control) to 123.5 mg N2 O-N m(-2) . Experiment III studied the effect of potworm density; we found that higher densities of potworms accelerated the peak of the N2 O emissions by 5 days (P < 0.001), but the cumulative N2 O emissions remained unaffected. We propose that increased soil aeration by the soil fauna reduced N2 O emissions in experiment I, whereas in experiment II N2 O emissions were driven by increased nitrogen and carbon availability. In experiment III, higher densities of potworms accelerated nitrogen and carbon availability and N2 O emissions, but did not increase them. Overall, our data show that soil fauna can suppress, increase, delay or accelerate N2 O emissions from soil and should therefore be an integral part of future N2 O studies.