Soil organic carbon loss decreases biodiversity but stimulates multitrophic interactions that promote belowground metabolism.

Soil organic carbon (SOC) plays an essential role in mediating community structure and metabolic activities of belowground biota. Unraveling the evolution of belowground communities and their feedback mechanisms on SOC dynamics helps embed the ecology of soil microbiome into carbon cycling, which serves to improve biodiversity conservation and carbon management strategy under global change. Here, croplands with a SOC gradient were used to understand how belowground metabolisms and SOC decomposition were linked to the diversity, composition, and co-occurrence networks of belowground communities encompassing archaea, bacteria, fungi, protists, and invertebrates. As SOC decreased, the diversity of prokaryotes and eukaryotes also decreased, but their network complexity showed contrasting patterns: prokaryotes increased due to intensified niche overlap, while that of eukaryotes decreased possibly because of greater dispersal limitation owing to the breakdown of macroaggregates. Despite the decrease in biodiversity and SOC stocks, the belowground metabolic capacity was enhanced as indicated by increased enzyme activity and decreased enzymatic stoichiometric imbalance. This could, in turn, expedite carbon loss through respiration, particularly in the slow-cycling pool. The enhanced belowground metabolic capacity was dominantly driven by greater multitrophic network complexity and particularly negative (competitive and predator-prey) associations, which fostered the stability of the belowground metacommunity. Interestingly, soil abiotic conditions including pH, aeration, and nutrient stocks, exhibited a less significant role. Overall, this study reveals a greater need for soil C resources across multitrophic levels to maintain metabolic functionality as declining SOC results in biodiversity loss. Our researchers highlight the importance of integrating belowground biological processes into models of SOC turnover, to improve agroecosystem functioning and carbon management in face of intensifying anthropogenic land-use and climate change.

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.

Community evolution increases plant productivity at low diversity.

Species extinctions from local communities negatively affect ecosystem functioning. Ecological mechanisms underlying these impacts are well studied, but the role of evolutionary processes is rarely assessed. Using a long-term field experiment, we tested whether natural selection in plant communities increased biodiversity effects on productivity. We re-assembled communities with 8-year co-selection history adjacent to communities with identical species composition but no history of co-selection ('naïve communities'). Monocultures, and in particular mixtures of two to four co-selected species, were more productive than their corresponding naïve communities over 4 years in soils with or without co-selected microbial communities. At the highest diversity level of eight plant species, no such differences were observed. Our findings suggest that plant community evolution can lead to rapid increases in ecosystem functioning at low diversity but may take longer at high diversity. This effect was not modified by treatments simulating co-evolutionary processes between plants and soil organisms.

Plant diversity maintains long-term ecosystem productivity under frequent drought by increasing short-term variation.

Increasing frequency of extreme climatic events can disrupt ecosystem processes and destabilize ecosystem functioning. Biodiversity may dampen these negative effects of environmental perturbations to provide greater ecosystem stability. We assessed the effects of plant diversity on the resistance, recovery and stability of experimental grassland ecosystems in response to recurring summer drought over 7 yr. Plant biomass production was reduced during the summer drought treatment compared with control plots. However, the negative effect of drought was relatively less pronounced at high than at low plant diversity, demonstrating that biodiversity increased ecosystem resistance to environmental perturbation. Furthermore, more diverse plant communities compensated for the reduced productivity during drought by increasing spring productivity compared to control plots. The drought-induced compensatory recovery led to increased short-term variations in productivity across growing seasons in more diverse communities that stabilized the longer-term productivity across years. Our findings show that short-term variation between seasons in the face of environmental perturbation can lead to longer-term stability of annual productivity in diverse ecosystems compared to less diverse ecosystems.

Root chemistry and soil fauna, but not soil abiotic conditions explain the effects of plant diversity on root decomposition.

Plant diversity influences many ecosystem functions including root decomposition. However, due to the presence of multiple pathways via which plant diversity may affect root decomposition, our mechanistic understanding of their relationships is limited. In a grassland biodiversity experiment, we simultaneously assessed the effects of three pathways-root litter quality, soil biota, and soil abiotic conditions-on the relationships between plant diversity (in terms of species richness and the presence/absence of grasses and legumes) and root decomposition using structural equation modeling. Our final structural equation model explained 70% of the variation in root mass loss. However, different measures of plant diversity included in our model operated via different pathways to alter root mass loss. Plant species richness had a negative effect on root mass loss. This was partially due to increased Oribatida abundance, but was weakened by enhanced root potassium (K) concentration in more diverse mixtures. Equally, grass presence negatively affected root mass loss. This effect of grasses was mostly mediated via increased root lignin concentration and supported via increased Oribatida abundance and decreased root K concentration. In contrast, legume presence showed a net positive effect on root mass loss via decreased root lignin concentration and increased root magnesium concentration, both of which led to enhanced root mass loss. Overall, the different measures of plant diversity had contrasting effects on root decomposition. Furthermore, we found that root chemistry and soil biota but not root morphology or soil abiotic conditions mediated these effects of plant diversity on root decomposition.

Soil biodiversity and soil community composition determine ecosystem multifunctionality.

Biodiversity loss has become a global concern as evidence accumulates that it will negatively affect ecosystem services on which society depends. So far, most studies have focused on the ecological consequences of above-ground biodiversity loss; yet a large part of Earth's biodiversity is literally hidden below ground. Whether reductions of biodiversity in soil communities below ground have consequences for the overall performance of an ecosystem remains unresolved. It is important to investigate this in view of recent observations that soil biodiversity is declining and that soil communities are changing upon land use intensification. We established soil communities differing in composition and diversity and tested their impact on eight ecosystem functions in model grassland communities. We show that soil biodiversity loss and simplification of soil community composition impair multiple ecosystem functions, including plant diversity, decomposition, nutrient retention, and nutrient cycling. The average response of all measured ecosystem functions (ecosystem multifunctionality) exhibited a strong positive linear relationship to indicators of soil biodiversity, suggesting that soil community composition is a key factor in regulating ecosystem functioning. Our results indicate that changes in soil communities and the loss of soil biodiversity threaten ecosystem multifunctionality and sustainability.

Plant diversity shapes microbe-rhizosphere effects on P mobilisation from organic matter in soil.

Plant species richness (PSR) increases nutrient uptake which depletes bioavailable nutrient pools in soil. No such relationship between plant uptake and availability in soil was found for phosphorus (P). We explored PSR effects on P mobilisation [phosphatase activity (PA)] in soil. PA increased with PSR. The positive PSR effect was not solely due to an increase in Corg concentrations because PSR remained significant if related to PA:Corg . An increase in PA per unit Corg increases the probability of the temporal and spatial match between substrate, enzyme and microorganism potentially serving as an adaption to competition. Carbon use efficiency of microorganisms (Cmic :Corg ) increased with increasing PSR while enzyme exudation efficiency (PA:Cmic ) remained constant. These findings suggest the need for efficient C rather than P cycling underlying the relationship between PSR and PA. Our results indicate that the coupling between C and P cycling in soil becomes tighter with increasing PSR.

The effect of successive summer drought periods on bacterial diversity along a plant species richness gradient.

Drought is a major stressor to soil microbial communities, and the intensification of climate change is predicted to increase hydric stress worldwide in the coming decades. As a possible mitigating factor for the consequences of prolonged drought periods, above and belowground biodiversity can increase ecosystem resistance and resilience by improving metabolic redundancy and complementarity as biodiversity increases. Here, we investigated the interaction effect between plant richness and successive, simulated summer drought on soil microbial communities during a period of 9 years.To do that, we made use of a well-established biodiversity experiment (The Jena Experiment) to investigate the response of microbial richness and community composition to successive drought periods alongside a plant richness gradient, which covers 1-, 2-, 4-, 8-, 16-, and 60-species plant communities. Plots were covered from natural precipitation by installing rain shelters 6 weeks every summer. Bulk soil samples were collected 1 year after the last summer drought was simulated. Our data indicate that bacterial richness increased after successive exposure to drought, with the increase being stable along the plant richness gradient. We identified a significant effect of plant species richness on the soil microbial community composition and determined the taxa significantly impacted by drought at each plant richness level. Our data successfully demonstrates that summer drought might have a legacy effect on soil bacterial communities.

Effects of inoculum additions in the presence of a preestablished arbuscular mycorrhizal fungal community.

Communities of arbuscular mycorrhizal fungi (AMF) are crucial for promoting plant productivity in most terrestrial systems, including anthropogenically managed ecosystems. Application of AMF inocula has therefore become a widespread practice. It is, however, pertinent to understand the mechanisms that govern AMF community composition and their performance in order to design successful manipulations. Here we assess whether the composition and plant growth-promotional effects of a synthetic AMF community can be altered by inoculum additions of the isolates forming the community. This was determined by following the effects of three AMF isolates, each inoculated in two propagule densities into a preestablished AMF community. Fungal abundance in roots and plant growth were evaluated in three sequential harvests. We found a transient positive response in AMF abundance to the intraspecific inoculation only in the competitively weakest isolate. The other two isolates responded negatively to intra- and interspecific inoculations, and in some cases plant growth was also reduced. Our results suggest that increasing the AMF density may lead to increased competition among fungi and a trade-off with their ability to promote plant productivity. This is a key ecological aspect to consider when introducing AMF into soils.

Drought-exposure history increases complementarity between plant species in response to a subsequent drought.

Growing threats from extreme climatic events and biodiversity loss have raised concerns about their interactive consequences for ecosystem functioning. Evidence suggests biodiversity can buffer ecosystem functioning during such climatic events. However, whether exposure to extreme climatic events will strengthen the biodiversity-dependent buffering effects for future generations remains elusive. We assess such transgenerational effects by exposing experimental grassland communities to eight recurrent summer droughts versus ambient conditions in the field. Seed offspring of 12 species are then subjected to a subsequent drought event in the glasshouse, grown individually, in monocultures or in 2-species mixtures. Comparing productivity between mixtures and monocultures, drought-selected plants show greater between-species complementarity than ambient-selected plants when recovering from the subsequent drought, causing stronger biodiversity effects on productivity and better recovery of drought-selected mixtures after the drought. These findings suggest exposure to recurrent climatic events can improve ecosystem responses to future events through transgenerational reinforcement of species complementarity.

Phylotype diversity within soil fungal functional groups drives ecosystem stability.

Soil fungi are fundamental to plant productivity, yet their influence on the temporal stability of global terrestrial ecosystems, and their capacity to buffer plant productivity against extreme drought events, remain uncertain. Here we combined three independent global field surveys of soil fungi with a satellite-derived temporal assessment of plant productivity, and report that phylotype richness within particular fungal functional groups drives the stability of terrestrial ecosystems. The richness of fungal decomposers was consistently and positively associated with ecosystem stability worldwide, while the opposite pattern was found for the richness of fungal plant pathogens, particularly in grasslands. We further demonstrated that the richness of soil decomposers was consistently positively linked with higher resistance of plant productivity in response to extreme drought events, while that of fungal plant pathogens showed a general negative relationship with plant productivity resilience/resistance patterns. Together, our work provides evidence supporting the critical role of soil fungal diversity to secure stable plant production over time in global ecosystems, and to buffer against extreme climate events.

Biodiversity-stability relationships strengthen over time in a long-term grassland experiment.

Numerous studies have demonstrated that biodiversity drives ecosystem functioning, yet how biodiversity loss alters ecosystems functioning and stability in the long-term lacks experimental evidence. We report temporal effects of species richness on community productivity, stability, species asynchrony, and complementarity, and how the relationships among them change over 17 years in a grassland biodiversity experiment. Productivity declined more rapidly in less diverse communities resulting in temporally strengthening positive effects of richness on productivity, complementarity, and stability. In later years asynchrony played a more important role in increasing community stability as the negative effect of richness on population stability diminished. Only during later years did species complementarity relate to species asynchrony. These results show that species complementarity and asynchrony can take more than a decade to develop strong stabilizing effects on ecosystem functioning in diverse plant communities. Thus, the mechanisms stabilizing ecosystem functioning change with community age.

Belowground biodiversity effects of plant symbionts support aboveground productivity.

Soil microbes play key roles in ecosystems, yet the impact of their diversity on plant communities is still poorly understood. Here we demonstrate that the diversity of belowground plant-associated soil fungi promotes plant productivity and plant coexistence. Using additive partitioning of biodiversity effects developed in plant biodiversity studies, we demonstrate that this positive relationship can be driven by complementarity effects among soil fungi in one soil type and by a selection effect resulting from the fungal species that stimulated plant productivity the most in another soil type. Selection and complementarity effects among fungal species contributed to improving plant productivity up to 82% and 85%, respectively, above the average of the respective fungal species monocultures depending on the soil in which they were grown. These results also indicate that belowground diversity may act as insurance for maintaining plant productivity under differing environmental conditions.

Mycorrhizal fungal identity and diversity relaxes plant-plant competition.

There is a great interest in ecology in understanding the role of soil microbial diversity for plant productivity and coexistence. Recent research has shown increases in species richness of mutualistic soil fungi, the arbuscular mycorrhizal fungi (AMF), to be related to increases in aboveground productivity of plant communities. However, the impact of AMF richness on plant-plant interactions has not been determined. Moreover, it is unknown whether species-rich AMF communities can act as insurance to maintain productivity in a fluctuating environment (e.g., upon changing soil conditions). We tested the impact of four different AMF taxa and of AMF diversity (no AMF, single AMF taxa, and all four together) on competitive interactions between the legume Trifolium pratense and the grass Lolium multiflorum grown under two different soil conditions of low and high sand content. We hypothesized that more diverse mutualistic interactions (e.g., when four AMF taxa are present) can ease competitive effects between plants, increase plant growth, and maintain plant productivity across different soil environments. We used quantitative PCR to verify that AMF taxa inoculated at the beginning of the experiment were still present at the end. The presence of AMF reduced the competitive inequality between the two plant species by reducing the growth suppression of the legume by the grass. High AMF richness enhanced the combined biomass production of the two plant species and the yield of the legume, particularly in the more productive soil with low sand content. In the less productive (high sand content) soil, the single most effective AMF had an equally beneficial effect on plant productivity as the mixture of four AMF. Since contributions of single AMF to plant productivity varied between both soils, higher AMF richness would be required to maintain plant productivity in heterogeneous environments. Overall this work shows that AMF diversity promotes plant productivity and that AMF diversity can act as insurance to sustain plant productivity under changing environmental conditions.

Diversity and asynchrony in soil microbial communities stabilizes ecosystem functioning.

Theoretical and empirical advances have revealed the importance of biodiversity for stabilizing ecosystem functions through time. Despite the global degradation of soils, whether the loss of soil microbial diversity can destabilize ecosystem functioning is poorly understood. Here, we experimentally quantified the contribution of soil fungal and bacterial communities to the temporal stability of four key ecosystem functions related to biogeochemical cycling. Microbial diversity enhanced the temporal stability of all ecosystem functions and this pattern was particularly strong in plant-soil mesocosms with reduced microbial richness where over 50% of microbial taxa were lost. The stabilizing effect of soil biodiversity was linked to asynchrony among microbial taxa whereby different soil fungi and bacteria promoted different ecosystem functions at different times. Our results emphasize the need to conserve soil biodiversity for the provisioning of multiple ecosystem functions that soils provide to the society.

Co-occurrence history increases ecosystem stability and resilience in experimental plant communities.

Understanding factors that maintain ecosystem stability is critical in the face of environmental change. Experiments simulating species loss from grassland have shown that losing biodiversity decreases ecosystem stability. However, as the originally sown experimental communities with reduced biodiversity develop, plant evolutionary processes or the assembly of interacting soil organisms may allow ecosystems to increase stability over time. We explored such effects in a long-term grassland biodiversity experiment with plant communities with either a history of co-occurrence (selected communities) or no such history (naïve communities) over a 4-yr period in which a major flood disturbance occurred. Comparing communities of identical species composition, we found that selected communities had temporally more stable biomass than naïve communities, especially at low species richness. Furthermore, selected communities showed greater biomass recovery after flooding, resulting in more stable post-flood productivity. In contrast to a previous study, the positive diversity-stability relationship was maintained after the flooding. Our results were consistent across three soil treatments simulating the presence or absence of co-selected microbial communities. We suggest that prolonged exposure of plant populations to a particular community context and abiotic site conditions can increase ecosystem temporal stability and resilience due to short-term evolution. A history of co-occurrence can in part compensate for species loss, as can high plant diversity in part compensate for the missing opportunity of such adaptive adjustments.

Crop cover is more important than rotational diversity for soil multifunctionality and cereal yields in European cropping systems.

In natural ecosystems, positive effects of plant diversity on ecosystem functioning have been widely observed, yet whether this is true in cropping systems remains unclear. Here we assessed the impact of crop diversification on soil microbial diversity, soil multifunctionality (SMF) and crop yields in 155 cereal fields across a 3,000 km north-south European gradient. Overall, crop diversity showed a relatively minor effect on soil microbial diversity, SMF and yields. In contrast, the proportion of time with crop cover (including cash crops, cover crops or forage leys) during the past ten-year crop rotation had a much stronger impact. This suggests that increasing crop cover can enhance both yields and soil functioning, while also providing habitat for soil microorganisms. We found that SMF did not positively contribute to crop yields, highlighting that care must be taken to balance the provision of food with environmentally beneficial functions and services, since they do not always go hand in hand.

Above- and belowground biodiversity jointly tighten the P cycle in agricultural grasslands.

Experiments showed that biodiversity increases grassland productivity and nutrient exploitation, potentially reducing fertiliser needs. Enhancing biodiversity could improve P-use efficiency of grasslands, which is beneficial given that rock-derived P fertilisers are expected to become scarce in the future. Here, we show in a biodiversity experiment that more diverse plant communities were able to exploit P resources more completely than less diverse ones. In the agricultural grasslands that we studied, management effects either overruled or modified the driving role of plant diversity observed in the biodiversity experiment. Nevertheless, we show that greater above- (plants) and belowground (mycorrhizal fungi) biodiversity contributed to tightening the P cycle in agricultural grasslands, as reduced management intensity and the associated increased biodiversity fostered the exploitation of P resources. Our results demonstrate that promoting a high above- and belowground biodiversity has ecological (biodiversity protection) and economical (fertiliser savings) benefits. Such win-win situations for farmers and biodiversity are crucial to convince farmers of the benefits of biodiversity and thus counteract global biodiversity loss.

Linkages between changes in plant and mycorrhizal fungal community composition at high versus low elevation in alpine ecosystems.

Arbuscular mycorrhizal fungi (AMF) play an important role in maintaining plant diversity and productivity in grassland ecosystems. However, very few studies have investigated how AMF and plant communities co-vary between contrasting environments in natural ecosystems. Intensive sampling (50 soil samples) was conducted in natural open grasslands at both 3570 and 4556 m on Mount Segrila on the Southeast Tibetan Plateau. We used 454-pyrosequencing to investigate soil AMF communities and to explore relationships between AMF diversity and plant richness, productivity and community composition. AMF diversity was negatively correlated with plant richness at 3570 m but positively at 4556 m. Differences in AMF community composition between elevations were attributable to plant community composition, soil pH and available phosphorus concentration. The AMF community was more phylogenetically clustered at the higher elevation than the lower elevation. However, greater phylogenetic clustering (under dispersion) of AMF communities at the two elevations was positively correlated with above-ground biomass. Our results indicate that plant community composition and environmental filtering are the primary drivers structuring the AMF community. Phylogenetic relatedness may be important in explaining the function of AMF communities in alpine ecosystems.

The results of biodiversity-ecosystem functioning experiments are realistic.

A large body of research shows that biodiversity loss can reduce ecosystem functioning. However, much of the evidence for this relationship is drawn from biodiversity-ecosystem functioning experiments in which biodiversity loss is simulated by randomly assembling communities of varying species diversity, and ecosystem functions are measured. This random assembly has led some ecologists to question the relevance of biodiversity experiments to real-world ecosystems, where community assembly or disassembly may be non-random and influenced by external drivers, such as climate, soil conditions or land use. Here, we compare data from real-world grassland plant communities with data from two of the largest and longest-running grassland biodiversity experiments (the Jena Experiment in Germany and BioDIV in the United States) in terms of their taxonomic, functional and phylogenetic diversity and functional-trait composition. We found that plant communities of biodiversity experiments cover almost all of the multivariate variation of the real-world communities, while also containing community types that are not currently observed in the real world. Moreover, they have greater variance in their compositional features than their real-world counterparts. We then re-analysed a subset of experimental data that included only ecologically realistic communities (that is, those comparable to real-world communities). For 10 out of 12 biodiversity-ecosystem functioning relationships, biodiversity effects did not differ significantly between the full dataset of biodiversity experiments and the ecologically realistic subset of experimental communities. Although we do not provide direct evidence for strong or consistent biodiversity-ecosystem functioning relationships in real-world communities, our results demonstrate that the results of biodiversity experiments are largely insensitive to the exclusion of unrealistic communities and that the conclusions drawn from biodiversity experiments are generally robust.