Showing papers by "Richard D. Bardgett published in 2019"

Soil nematode abundance and functional group composition at a global scale

Abstract: Soil organisms are a crucial part of the terrestrial biosphere. Despite their importance for ecosystem functioning, few quantitative, spatially explicit models of the active belowground community currently exist. In particular, nematodes are the most abundant animals on Earth, filling all trophic levels in the soil food web. Here we use 6,759 georeferenced samples to generate a mechanistic understanding of the patterns of the global abundance of nematodes in the soil and the composition of their functional groups. The resulting maps show that 4.4 ± 0.64 × 1020 nematodes (with a total biomass of approximately 0.3 gigatonnes) inhabit surface soils across the world, with higher abundances in sub-Arctic regions (38% of total) than in temperate (24%) or tropical (21%) regions. Regional variations in these global trends also provide insights into local patterns of soil fertility and functioning. These high-resolution models provide the first steps towards representing soil ecological processes in global biogeochemical models and will enable the prediction of elemental cycling under current and future climate scenarios.

A few Ascomycota taxa dominate soil fungal communities worldwide

Abstract: Despite having key functions in terrestrial ecosystems, information on the dominant soil fungi and their ecological preferences at the global scale is lacking. To fill this knowledge gap, we surveyed 235 soils from across the globe. Our findings indicate that 83 phylotypes (<0.1% of the retrieved fungi), mostly belonging to wind dispersed, generalist Ascomycota, dominate soils globally. We identify patterns and ecological drivers of dominant soil fungal taxa occurrence, and present a map of their distribution in soils worldwide. Whole-genome comparisons with less dominant, generalist fungi point at a significantly higher number of genes related to stress-tolerance and resource uptake in the dominant fungi, suggesting that they might be better in colonising a wide range of environments. Our findings constitute a major advance in our understanding of the ecology of fungi, and have implications for the development of strategies to preserve them and the ecosystem functions they provide.

Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems

Abstract: Plant-soil feedbacks (PSFs) are interactions among plants, soil organisms, and abiotic soil conditions that influence plant performance, plant species diversity, and community structure, ultimately driving ecosystem processes. We review how climate change will alter PSFs and their potential consequences for ecosystem functioning. Climate change influences PSFs through the performance of interacting species and altered community composition resulting from changes in species distributions. Climate change thus affects plant inputs into the soil subsystem via litter and rhizodeposits and alters the composition of the living plant roots with which mutualistic symbionts, decomposers, and their natural enemies interact. Many of these plant-soil interactions are species-specific and are greatly affected by temperature, moisture, and other climate-related factors. We make a number of predictions concerning climate change effects on PSFs and consequences for vegetation-soil-climate feedbacks while acknowledging that they may be context-dependent, spatially heterogeneous, and temporally variable.

Changes in belowground biodiversity during ecosystem development.

Abstract: Belowground organisms play critical roles in maintaining multiple ecosystem processes, including plant productivity, decomposition, and nutrient cycling. Despite their importance, however, we have a limited understanding of how and why belowground biodiversity (bacteria, fungi, protists, and invertebrates) may change as soils develop over centuries to millennia (pedogenesis). Moreover, it is unclear whether belowground biodiversity changes during pedogenesis are similar to the patterns observed for aboveground plant diversity. Here we evaluated the roles of resource availability, nutrient stoichiometry, and soil abiotic factors in driving belowground biodiversity across 16 soil chronosequences (from centuries to millennia) spanning a wide range of globally distributed ecosystem types. Changes in belowground biodiversity during pedogenesis followed two main patterns. In lower-productivity ecosystems (i.e., drier and colder), increases in belowground biodiversity tracked increases in plant cover. In more productive ecosystems (i.e., wetter and warmer), increased acidification during pedogenesis was associated with declines in belowground biodiversity. Changes in the diversity of bacteria, fungi, protists, and invertebrates with pedogenesis were strongly and positively correlated worldwide, highlighting that belowground biodiversity shares similar ecological drivers as soils and ecosystems develop. In general, temporal changes in aboveground plant diversity and belowground biodiversity were not correlated, challenging the common perception that belowground biodiversity should follow similar patterns to those of plant diversity during ecosystem development. Taken together, our findings provide evidence that ecological patterns in belowground biodiversity are predictable across major globally distributed ecosystem types and suggest that shifts in plant cover and soil acidification during ecosystem development are associated with changes in belowground biodiversity over centuries to millennia.

Microbial responses to warming enhance soil carbon loss following translocation across a tropical forest elevation gradient

Abstract: Tropical soils contain huge carbon stocks, which climate warming is projected to reduce by stimulating organic matter decomposition, creating a positive feedback that will promote further warming. Models predict that the loss of carbon from warming soils will be mediated by microbial physiology, but no empirical data are available on the response of soil carbon and microbial physiology to warming in tropical forests, which dominate the terrestrial carbon cycle. Here we show that warming caused a considerable loss of soil carbon that was enhanced by associated changes in microbial physiology. By translocating soils across a 3000 m elevation gradient in tropical forest, equivalent to a temperature change of ± 15 °C, we found that soil carbon declined over 5 years by 4% in response to each 1 °C increase in temperature. The total loss of carbon was related to its original quantity and lability, and was enhanced by changes in microbial physiology including increased microbial carbon-use-efficiency, shifts in community composition towards microbial taxa associated with warmer temperatures, and increased activity of hydrolytic enzymes. These findings suggest that microbial feedbacks will cause considerable loss of carbon from tropical forest soils in response to predicted climatic warming this century.

High throughput method for measuring urease activity in soil.

Abstract: Extracellular enzymes break down soil organic matter into smaller compounds and their measurement has proved to be a powerful tool to evaluate the functionality of soils. Urease is the enzyme that degrades urea and is widely considered to be a good proxy of nitrogen (N) mineralisation. But the methods available to measure this enzyme are time consuming; as such, urease is not commonly included in standard enzyme profiling of soils. We developed a fast, high throughput and reproducible colorimetric microplate technique to evaluate urease activity in soil. The method involves the incubation of soil slurries in 96-deepwell blocks with urea solutions and the measurement, by colorimetric reaction, of ammonium produced. We compared the new method with existing methods, yielding comparable results, and evaluated optimal conditions for urease analysis (soil slurry concentration, substrate concentration, incubation times and extractant salt concentration) in different grassland soils. The method proved to be a faster, higher throughput, and more precise alternative to existing methods for evaluating this important N-related enzyme.

Relationships between plant traits, soil properties and carbon fluxes differ between monocultures and mixed communities in temperate grassland

Abstract: The use of plant traits to predict ecosystem functions has been gaining growing attention. Above-ground plant traits, such as leaf nitrogen (N) content and specific leaf area (SLA), have been shown to strongly relate to ecosystem productivity, respiration and nutrient cycling. Furthermore, increasing plant functional trait diversity has been suggested as a possible mechanism to increase ecosystem carbon (C) storage. However, it is uncertain whether below-ground plant traits can be predicted by above-ground traits, and if both above- and below-ground traits can be used to predict soil properties and ecosystem-level functions. Here, we used two adjacent field experiments in temperate grassland to investigate if above- and below-ground plant traits are related, and whether relationships between plant traits, soil properties and ecosystem C fluxes (i.e. ecosystem respiration and net ecosystem exchange) measured in potted monocultures could be detected in mixed field communities. We found that certain shoot traits (e.g. shoot N and C, and leaf dry matter content) were related to root traits (e.g. root N, root C:N and root dry matter content) in monocultures, but such relationships were either weak or not detected in mixed communities. Some relationships between plant traits (i.e. shoot N, root N and/or shoot C:N) and soil properties (i.e. inorganic N availability and microbial community structure) were similar in monocultures and mixed communities, but they were more strongly linked to shoot traits in monocultures and root traits in mixed communities. Structural equation modelling showed that above- and below-ground traits and soil properties improved predictions of ecosystem C fluxes in monocultures, but not in mixed communities on the basis of community-weighted mean traits. Synthesis. Our results from a single grassland habitat detected relationships in monocultures between above- and below-ground plant traits, and between plant traits, soil properties and ecosystem C fluxes. However, these relationships were generally weaker or different in mixed communities. Our results demonstrate that while plant traits can be used to predict certain soil properties and ecosystem functions in monocultures, they are less effective for predicting how changes in plant species composition influence ecosystem functions in mixed communities.

Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic

Abstract: In contrast to the situation in plants inhabiting most of the world's ecosystems, mycorrhizal fungi are usually absent from roots of the only two native vascular plant species of maritime Antarctica, Deschampsia antarctica and Colobanthus quitensis. Instead, a range of ascomycete fungi, termed dark septate endophytes (DSEs), frequently colonise the roots of these plant species. We demonstrate that colonisation of Antarctic vascular plants by DSEs facilitates not only the acquisition of organic nitrogen as early protein breakdown products, but also as non-proteinaceous d-amino acids and their short peptides, accumulated in slowly-decomposing organic matter, such as moss peat. Our findings suggest that, in a warming maritime Antarctic, this symbiosis has a key role in accelerating the replacement of formerly dominant moss communities by vascular plants, and in increasing the rate at which ancient carbon stores laid down as moss peat over centuries or millennia are returned to the atmosphere as CO2 .

Using plant, microbe and soil fauna traits to improve the predictive power of biogeochemical models

Abstract: ELF is supported by the NERC Soil Security Programme (NE/P013708/1); JRD and BGJ by the UK Biotechnology and Biological Sciences Research Council (BBSRC) (Grants BB/I009000/2 and BB/I009183/1) DJ receives partial support from the N8 AgriFood programme This work was supported by a BBSRC International Partnering award (BB/L026759/1) to EB, DJ, RB and PS

Drought decreases incorporation of recent plant photosynthate into soil food webs regardless of their trophic complexity

Abstract: Theory suggests that more complex food webs promote stability and can buffer the effects of perturbations, such as drought, on soil organisms and ecosystem functions. Here, we tested experimentally how soil food web trophic complexity modulates the response to drought of soil functions related to carbon cycling and the capture and transfer below-ground of recent photosynthate by plants. We constructed experimental systems comprising soil communities with one, two or three trophic levels (microorganisms, detritivores and predators) and subjected them to drought. We investigated how food web trophic complexity in interaction with drought influenced litter decomposition, soil CO2 efflux, mycorrhizal colonization, fungal production, microbial communities and soil fauna biomass. Plants were pulse-labelled after the drought with 13 C-CO2 to quantify the capture of recent photosynthate and its transfer below-ground. Overall, our results show that drought and soil food web trophic complexity do not interact to affect soil functions and microbial community composition, but act independently, with an overall stronger effect of drought. After drought, the net uptake of 13 C by plants was reduced and its retention in plant biomass was greater, leading to a strong decrease in carbon transfer below-ground. Although food web trophic complexity influenced the biomass of Collembola and fungal hyphal length, 13 C enrichment and the net transfer of carbon from plant shoots to microbes and soil CO2 efflux were not affected significantly by varying the number of trophic groups. Our results indicate that drought has a strong effect on above-ground-below-ground linkages by reducing the flow of recent photosynthate. Our results emphasize the sensitivity of the critical pathway of recent photosynthate transfer from plants to soil organisms to a drought perturbation, and show that these effects may not be mitigated by the trophic complexity of soil communities, at least at the level manipulated in this experiment.

Grassland biodiversity restoration increases resistance of carbon fluxes to drought

Abstract: Evidence suggests that the restoration of plant diversity in grasslands not only brings benefits for biodiversity conservation, but also the delivery of ecosystem services. While biodiversity-function experiments show that greater plant diversity increases resistance of plant productivity to climate extremes, it is not known whether real-world management options for grassland restoration likewise stabilize ecosystem responses to extreme climate events. We used a long-term (23 year) field experiment in northern England to test the hypothesis that management aimed at biodiversity restoration increases the resistance and recovery of ecosystem carbon (C) fluxes to short-term summer drought. This was tested by measuring plant, soil and microbial responses to a simulated drought in experimental grassland plots where fertilizer application and seed addition have been managed to enhance plant species diversity. The cessation of fertilizer application brought about small increases in plant species richness. Additionally, cessation of fertilizer application reduced overall plant productivity and promoted hemi-parasitic plants at the expense of grasses and forbs. Resistance of CO 2 fluxes to drought, measured as ecosystem respiration, was greater in non-fertilized plots, as lower plant biomass reduced water demand, likely aided by proportionally more hemi-parasitic plants further reducing plant biomass. Additionally, legumes increased under drought, thereby contributing to overall resistance of plant productivity. Recovery of soil microbial C and nitrogen was more rapid after rewetting than soil microbial community composition, irrespective of restoration treatment, suggesting high resilience of soil microbial communities to drought. Synthesis and applications. This study shows that while grassland diversity restoration management increases the resistance of carbon fluxes to drought, it also reduces agricultural yields, revealing a trade-off for land managers. Furthermore legumes, promoted through long-term restoration treatments, can help to maintain plant community productivity under drought by increasing their biomass. As such, grassland management strategies not only have consequences for ecosystem processes, but also the capacity to withstand extreme weather events.

Towards more predictive and interdisciplinary climate change ecosystem experiments

Abstract: Despite great advances, experiments concerning the response of ecosystems to climate change still face considerable challenges, including the high complexity of climate change in terms of environmental variables, constraints in the number and amplitude of climate treatment levels, and the limited scope of responses and interactions covered. Drawing on the expertise of researchers from a variety of disciplines, this Perspective outlines how computational and technological advances can help in designing experiments that can contribute to overcoming these challenges, and also outlines a first application of such an experimental design.

Plastic and genetic responses of a common sedge to warming have contrasting effects on carbon cycle processes

Abstract: Climate warming affects plant physiology through genetic adaptation and phenotypic plasticity, but little is known about how these mechanisms influence ecosystem processes. We used three elevation gradients and a reciprocal transplant experiment to show that temperature causes genetic change in the sedge Eriophorum vaginatum. We demonstrate that plants originating from warmer climate produce fewer secondary compounds, grow faster and accelerate carbon dioxide (CO2 ) release to the atmosphere. However, warmer climate also caused plasticity in E. vaginatum, inhibiting nitrogen metabolism, photosynthesis and growth and slowing CO2 release into the atmosphere. Genetic differentiation and plasticity in E. vaginatum thus had opposing effects on CO2 fluxes, suggesting that warming over many generations may buffer, or reverse, the short-term influence of this species over carbon cycle processes. Our findings demonstrate the capacity for plant evolution to impact ecosystem processes, and reveal a further mechanism through which plants will shape ecosystem responses to climate change.

Drought soil legacy overrides maternal effects on plant growth

Abstract: Maternal effects (i.e. trans-generational plasticity) and soil legacies generated by drought and plant diversity can affect plant performance and alter nutrient cycling and plant community dynamics. However, the relative importance and combined effects of these factors on plant growth dynamics remain poorly understood. We used soil and seeds from an existing plant diversity and drought manipulation field experiment in temperate grassland to test maternal, soil drought and diversity legacy effects, and their interactions, on offspring plant performance of two grassland species (Alopecurus pratensis and Holcus lanatus) under contrasting glasshouse conditions. Our results showed that drought soil legacy effects eclipsed maternal effects on plant biomass. Drought soil legacy effects were attributed to changes in both abiotic (i.e. nutrient availability) and biotic soil properties (i.e. microbial carbon and enzyme activity), as well as plant root and shoot atom 15N excess. Further, plant tissue nutrient concentrations and soil microbial C:N responses to drought legacies varied between the two plant species and soils from high and low plant diversity treatments. However, these diversity effects did not affect plant root or shoot biomass. These findings demonstrate that while maternal effects resulting from drought occur in grasslands, their impacts on plant performance are likely minor relative to drought legacy effects on soil abiotic and biotic properties. This suggests that soil drought legacy effects could become increasingly important drivers of plant community dynamics and ecosystem functioning as extreme weather events become more frequent and intense with climate change. A plain language summary is available for this article.

Soil biota, carbon cycling and crop plant biomass responses to biochar in a temperate mesocosm experiment

Abstract: Biochar addition to soil is a carbon capture and storage option with potential to mitigate rising atmospheric CO2 concentrations, yet the consequences for soil organisms and linked ecosystem processes are inconsistent or unknown. We tested biochar impact on soil biodiversity, ecosystem functions, and their interactions, in temperate agricultural soils. We performed a 27-month factorial experiment to determine effects of biochar, soil texture, and crop species treatments on microbial biomass (PFLA), soil invertebrate density, crop biomass and ecosystem CO2 flux in plant-soil mesocosms. Overall soil microbial biomass, microarthropod abundance and crop biomass were unaffected by biochar, although there was an increase in fungal-bacterial ratio and a positive relationship between the 16:1ω5 fatty acid marker of AMF mass and collembolan density in the biochar-treated mesocosms. Ecosystem CO2 fluxes were unaffected by biochar, but soil carbon content of biochar-treated mesocosms was significantly lower, signifying a possible movement/loss of biochar or priming effect. Compared to soil texture and crop type, biochar had minimal impact on soil biota, crop production and carbon cycling. Future research should examine subtler effects of biochar on biotic regulation of ecosystem production and if the apparent robustness to biochar weakens over greater time spans or in combination with other ecological perturbations.

Blind spots in global soil biodiversity and ecosystem function research

Abstract: Soils harbor a substantial fraction of the world’s biodiversity, contributing to many crucial ecosystem functions. It is thus essential to identify general macroecological patterns related to the distribution and functioning of soil organisms to support their conservation and governance. Here we identify and characterize the existing gaps in soil biodiversity and ecosystem function data across soil macroecological studies and >11,000 sampling sites. These include significant spatial, environmental, taxonomic, and functional gaps, and an almost complete absence of temporally explicit data. We also identify the limitations of soil macroecological studies to explore general patterns in soil biodiversity-ecosystem functioning relationships, with only 0.6% of all sampling sites having a non-systematic coverage of both biodiversity and function datasets. Based on this information, we provide clear priorities to support and expand soil macroecological research.

Applying the aboveground-belowground interaction concept in agriculture: Spatio-temporal scales matter

Abstract: Interactions between aboveground and belowground organisms are important drivers of plant growth and performance in natural ecosystems. Making practical use of such above-belowground biotic interactions offers important opportunities for enhancing the sustainability of agriculture, as it could favor crop growth, nutrient supply, and defense against biotic and abiotic stresses. However, the operation of above-and belowground organisms at different spatial and temporal scales provides important challenges for application in agriculture. Aboveground organisms, such as herbivores and pollinators, operate at spatial scales that exceed individual fields and are highly variable in abundance within growing seasons. In contrast, pathogenic, symbiotic, and decomposer soil biota operate at more localized spatial scales from individual plants to patches of square meters, however, they generate legacy effects on plant performance that may last from single to multiple years. The challenge is to promote pollinators and suppress pests at the landscape and field scale, while creating positive legacy effects of local plant-soil interactions for next generations of plants. Here, we explore the possibilities to improve utilization of above-belowground interactions in agro-ecosystems by considering spatio-temporal scales at which aboveground and belowground organisms operate. We identified that successful integration of above-belowground biotic interactions initially requires developing crop rotations and intercropping systems that create positive local soil legacy effects for neighboring as well subsequent crops. These configurations may then be used as building blocks to design landscapes that accommodate beneficial aboveground communities with respect to their required resources. For successful adoption of above-belowground interactions in agriculture there is a need for context-specific solutions, as well as sound socio-economic embedding.

Author Correction: Evolutionary history resolves global organization of root functional traits.

Abstract: We thank reader Joseph Craine for pointing out three inadvertent errors in this Letter. First, 4 of the 71 divergence dates extracted from ref. 1 of this Amendment and used in Fig. 1b of the original Letter were overestimated. The correct values are 45 million years ago (Ma) for Apocynaceae, 51 Ma for Anacardiaceae, 40 Ma for Primulaceae, and 53 Ma for Amaryllidaceae. These errors had little influence on the overall trend of Fig. 1b (r2 is now 0.48 rather than 0.54, with no change to P < 0.001) and do not change our conclusion and inferences. Second, we neglected to note that since refs. 1 and 2 of this Amendment considered only angiosperms, our Fig. 1b necessarily did not include gymnosperm taxa. The in-text reference to Fig. 1b should therefore read “all major angiosperm plant families in our dataset” rather than “all major vascular plant families in our dataset”. Third, in Fig. 1c the trait value of mycorrhizal colonization for Machilus kwangtungensis was erroneously given the value 0.25 instead of 1.0. This error had little influence on the overall Fig. 1c trend, reducing r2 from 0.64 to 0.63 (with no change to P < 0.001).

Guiding carbon farming using interdisciplinary mixed methods mapping

Abstract: In recognition of the need to address complex environmental problems, some ecological studies have adopted social research methods to better understand the complexity of social‐ecological systems management. The overwhelming majority of these studies stop short of fully embracing qualitative methodologies. The lack of integrative social and natural science data for a topic such as soil carbon farming is problematic as theoretical carbon sequestration opportunities identified through soil mapping and process‐based models can fail to deliver the sequestration levels promised when introduced on‐the‐ground. Such mapping needs to account for the human factors involved in delivering increased soil carbon on‐farm. Here, we develop a mixed methods mapping approach to explore the potential for increasing soil carbon stocks on upland farms in the UK. Our approach considers ecological and social complexity through application of soil science, ecology, participant observation, interviews and a focus group. Our maps revealed landscapes that are full of carbon farming opportunity, but contain previously hidden barriers to the delivery of increased soil carbon. For example, they revealed that carbon farming can be considered by farmers to work in opposition to perceived ‘good farming’ practices and be correlated with increased incidents of livestock disease. We also discovered that the use of maps in research can be problematic as they can close down discussion and exclude local representation of an area. Trialling an interdisciplinary mixed methods approach produced new, deeper and more richly‐textured understandings about how soil carbon management is produced socially as well as ecologically on upland livestock farms. Our findings have potential to improve the success of future carbon farming initiatives by incorporating farmer knowledge and social drivers of implementation.

Ecological niche differentiation in soil cyanobacterial communities across the globe

Abstract: Cyanobacteria are key organisms in the evolution of life on Earth, but their distribution and environmental preferences in terrestrial ecosystems remain poorly understood. This lack of knowledge is particularly evident for two recently discovered non-photosynthetic cyanobacterial classes, Melainabacteria and Sericytochromatia, limiting our capacity to predict how these organisms and the important ecosystem functions they perform will respond to ongoing global change. Here, we conducted a global field survey covering a wide range of vegetation types and climatic conditions to identify the environmental factors associated with the distribution of soil cyanobacterial communities. Network analyses revealed three major clusters of cyanobacterial phylotypes, each one dominated by members of one of the extant classes of Cyanobacteria (Oxyphotobacteria, Melainabacteria and Sericytochromatia), suggesting that species within these taxonomic groups share similar environmental preferences. Melainabacteria appear mostly in acidic and humid ecosystems, especially forests, Oxyphotobacteria are prevalent in arid and semiarid areas, and Sericytochromatia are common in hyperarid oligotrophic environments. We used this information to construct a global atlas of soil cyanobacteria. Our results provide novel insights into the ecology and biogeography of soil cyanobacteria and highlight how their global distribution could change in response to increased aridity, a landmark feature of climate change in terrestrial ecosystems worldwide