Interactions between climate warming and land management regulate greenhouse gas fluxes in a temperate grassland ecosystem.

Greenhouse gas (GHG) fluxes from grasslands are affected by climate warming and agricultural management practices including nitrogen (N) fertiliser application and grazing. However, the interactive effects of these factors are poorly resolved in field studies. We used a factorial in situ experiment - combining warming, N-fertiliser and above-ground cutting treatments - to explore their individual and interactive effects on plant-soil properties and GHG fluxes in a temperate UK grassland over two years. Our results showed no interactive treatment effects on plant productivity despite individual effects of N-fertiliser and warming on above- and below-ground biomass. There were, however, interactive treatment effects on GHG fluxes that varied across the two years. In year 1, warming and N-fertiliser increased CO2 and reduced N2O fluxes. N-fertilised also interacted with above-ground biomass (AGB) removal increasing N2O fluxes in year one and reducing CO2 fluxes in year two. The grassland was consistently a sink of CH4; N-fertilised increased the sink by 45% (year 1), AGB removal and warming reduced CH4 consumption by 44% and 43%, respectively (year 2). The majority of the variance in CO2 fluxes was explained by above-ground metrics (grassland productivity and leaf dry matter content), with microclimate (air and soil temperature and soil moisture) and below-ground (root N content) metrics also significant. Soil chemistry (soil mineral N and net mineralisation rate), below-ground (specific root length) and microclimate (soil moisture) metrics explained 49% and 24% of the variance in N2O and CH4 fluxes, respectively. Overall, our work demonstrates the importance of interactions between climate and management as determinants of short-term grassland GHG fluxes. These results show that reduced cutting combined with lower inorganic N-fertilisers would constrain grassland C and N cycling and GHG fluxes in warmer climatic conditions. This has implications for strategic grassland management decisions to mitigate GHG fluxes in a warming world.

Land-use changes alter soil bacterial composition and diversity in tropical forest soil in China.

Tropical forests, under pressure from human activities, are important reservoirs of biodiversity and regulators of global biogeochemical cycles. Land-use and management are influential drivers of environmental change and ecosystem sustainability. However, only limited studies have analysed the impacts of planting age and vegetation type under land-use change on soil microbial community in tropical forests simultaneously. Here, we assessed soil bacterial community composition and diversity under different land-use in Hainan Province, China, using high-throughput sequencing combined with PICRUSt analysis. Land-use included natural forest, 5-year-old cropland, young (5-year-old) rubber tree plantation, and old (30-year-old) rubber tree plantation. Land-use changes altered the soil bacterial community composition but had a non-significant influence on alpha diversity (P > .05). We found that bacterial beta-diversity significantly decreased in young rubber tree plantation soils and cropland soils compared to natural forest as a control. In contrast, soil bacterial beta-diversity increased in old rubber tree plantation soils, indicating the effects of time since planting. There was no difference in microbial beta-diversity between soils from cropland and young rubber tree plantation. Soil bulk density and moisture, not pH, were the main environmental factors explaining the variability in microbial diversity. PICRUSt analysis of soil bacterial predicted gene abundances within metabolic pathways and indicated that land-use change altered soil functional traits, e.g., amino acid-related enzymes, ribosomes, DNA repair/recombination proteins and oxidative phosphorylation. Also, vegetation type, not planting age, had significant impacts on soil functional traits. Overall, planting age had the greatest influence on soil bacterial beta-diversity, while vegetation type was more crucial for soil functional traits (P < .05).

Drought soil legacy overrides maternal effects on plant growth.

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.

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

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.

Logging and soil nutrients independently explain plant trait expression in tropical forests.

Plant functional traits regulate ecosystem functions but little is known about how co-occurring gradients of land use and edaphic conditions influence their expression. We test how gradients of logging disturbance and soil properties relate to community-weighted mean traits in logged and old-growth tropical forests in Borneo. We studied 32 physical, chemical and physiological traits from 284 tree species in eight 1 ha plots and measured long-term soil nutrient supplies and plant-available nutrients. Logged plots had greater values for traits that drive carbon capture and growth, whilst old-growth forests had greater values for structural and persistence traits. Although disturbance was the primary driver of trait expression, soil nutrients explained a statistically independent axis of variation linked to leaf size and nutrient concentration. Soil characteristics influenced trait expression via nutrient availability, nutrient pools, and pH. Our finding, that traits have dissimilar responses to land use and soil resource availability, provides robust evidence for the need to consider the abiotic context of logging when predicting plant functional diversity across human-modified tropical forests. The detection of two independent axes was facilitated by the measurement of many more functional traits than have been examined in previous studies.

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

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.

Fungal diversity regulates plant-soil feedbacks in temperate grassland.

Feedbacks between plants and soil microbial communities play an important role in vegetation dynamics, but the underlying mechanisms remain unresolved. Here, we show that the diversity of putative pathogenic, mycorrhizal, and saprotrophic fungi is a primary regulator of plant-soil feedbacks across a broad range of temperate grassland plant species. We show that plant species with resource-acquisitive traits, such as high shoot nitrogen concentrations and thin roots, attract diverse communities of putative fungal pathogens and specialist saprotrophs, and a lower diversity of mycorrhizal fungi, resulting in strong plant growth suppression on soil occupied by the same species. Moreover, soil properties modulate feedbacks with fertile soils, promoting antagonistic relationships between soil fungi and plants. This study advances our capacity to predict plant-soil feedbacks and vegetation dynamics by revealing fundamental links between soil properties, plant resource acquisition strategies, and the diversity of fungal guilds in soil.

Soil multifunctionality and drought resistance are determined by plant structural traits in restoring grassland.

It is increasingly recognized that belowground responses to vegetation change are closely linked to plant functional traits. However, our understanding is limited concerning the relative importance of different plant traits for soil functions and of the mechanisms by which traits influence soil properties in the real world. Here we test the hypothesis that taller species, or those with complex rooting structures, are associated with high rates of nutrient and carbon (C) cycling in grassland. We further hypothesized that communities dominated by species with deeper roots may be more resilient to drought. These hypotheses were tested in a 3-yr grassland restoration experiment on degraded ex-arable land in southern England. We sowed three trait-based plant functional groups, assembled using database derived values of plant traits, and their combinations into bare soil. This formed a range of plant trait syndromes onto which we superimposed a simulated drought 2 yr after initial establishment. We found strong evidence that community weighted mean (CWM) of plant height is negatively associated with soil nitrogen cycling and availability and soil multifunctionality. We propose that this was due to an exploitative resource capture strategy that was inappropriate in shallow chalk soils. Further, complexity of root architecture was positively related to soil multifunctionality throughout the season, with fine fibrous roots being associated with greater rates of nutrient cycling. Drought resistance of soil functions including ecosystem respiration, mineralization, and nitrification were positively related to functional divergence of rooting depth, indicating that, in shallow chalk soils, a range of water capture strategies is necessary to maintain functions. Finally, after 3 yr of the experiment, we did not detect any links between the plant traits and microbial communities, supporting the finding that traits based on plant structure and resource foraging capacity are the main variables driving soil function in the early years of grassland conversion. We suggest that screening recently restored grassland communities for potential soil multifunctionality and drought resilience may be possible based on rooting architecture and plant height. These results indicate that informed assembly of plant communities based on plant traits could aid in the restoration of functioning in degraded soil.

Predicting the structure of soil communities from plant community taxonomy, phylogeny, and traits.

There are numerous ways in which plants can influence the composition of soil communities. However, it remains unclear whether information on plant community attributes, including taxonomic, phylogenetic, or trait-based composition, can be used to predict the structure of soil communities. We tested, in both monocultures and field-grown mixed temperate grassland communities, whether plant attributes predict soil communities including taxonomic groups from across the tree of life (fungi, bacteria, protists, and metazoa). The composition of all soil community groups was affected by plant species identity, both in monocultures and in mixed communities. Moreover, plant community composition predicted additional variation in soil community composition beyond what could be predicted from soil abiotic characteristics. In addition, analysis of the field aboveground plant community composition and the composition of plant roots suggests that plant community attributes are better predictors of soil communities than root distributions. However, neither plant phylogeny nor plant traits were strong predictors of soil communities in either experiment. Our results demonstrate that grassland plant species form specific associations with soil community members and that information on plant species distributions can improve predictions of soil community composition. These results indicate that specific associations between plant species and complex soil communities are key determinants of biodiversity patterns in grassland soils.

Biogeographic differences in soil biota promote invasive grass response to nutrient addition relative to co-occurring species despite lack of belowground enemy release.

Multiple plant species invasions and increases in nutrient availability are pervasive drivers of global environmental change that often co-occur. Many plant invasion studies, however, focus on single-species or single-mechanism invasions, risking an oversimplification of a multifaceted process. Here, we test how biogeographic differences in soil biota, such as belowground enemy release, interact with increases in nutrient availability to influence invasive plant growth. We conducted a greenhouse experiment using three co-occurring invasive grasses and one native grass. We grew species in live and sterilized soil from the invader's native (United Kingdom) and introduced (New Zealand) ranges with a nutrient addition treatment. We found no evidence for belowground enemy release. However, species' responses to nutrients varied, and this depended on soil origin and sterilization. In live soil from the introduced range, the invasive species Lolium perenne L. responded more positively to nutrient addition than co-occurring invasive and native species. In contrast, in live soil from the native range and in sterilized soils, there were no differences in species' responses to nutrients. This suggests that the presence of soil biota from the introduced range allowed L. perenne to capture additional nutrients better than co-occurring species. Considering the globally widespread nature of anthropogenic nutrient additions to ecosystems, this effect could be contributing to a global homogenization of flora and the associated losses in native species diversity.

Belowground competition drives invasive plant impact on native species regardless of nitrogen availability.

Plant invasions and eutrophication are pervasive drivers of global change that cause biodiversity loss. Yet, how invasive plant impacts on native species, and the mechanisms underpinning these impacts, vary in relation to increasing nitrogen (N) availability remains unclear. Competition is often invoked as a likely mechanism, but the relative importance of the above and belowground components of this is poorly understood, particularly under differing levels of N availability. To help resolve these issues, we quantified the impact of a globally invasive grass species, Agrostis capillaris, on two co-occurring native New Zealand grasses, and vice versa. We explicitly separated above- and belowground interactions amongst these species experimentally and incorporated an N addition treatment. We found that competition with the invader had large negative impacts on native species growth (biomass decreased by half), resource capture (total N content decreased by up to 75%) and even nutrient stoichiometry (native species tissue C:N ratios increased). Surprisingly, these impacts were driven directly and indirectly by belowground competition, regardless of N availability. Higher root biomass likely enhanced the invasive grass's competitive superiority belowground, indicating that root traits may be useful tools for understanding invasive plant impacts. Our study shows that belowground competition can be more important in driving invasive plant impacts than aboveground competition in both low and high fertility ecosystems, including those experiencing N enrichment due to global change. This can help to improve predictions of how two key drivers of global change, plant species invasions and eutrophication, impact native species diversity.

Vascular plants promote ancient peatland carbon loss with climate warming.

Northern peatlands have accumulated one third of the Earth's soil carbon stock since the last Ice Age. Rapid warming across northern biomes threatens to accelerate rates of peatland ecosystem respiration. Despite compensatory increases in net primary production, greater ecosystem respiration could signal the release of ancient, century- to millennia-old carbon from the peatland organic matter stock. Warming has already been shown to promote ancient peatland carbon release, but, despite the key role of vegetation in carbon dynamics, little is known about how plants influence the source of peatland ecosystem respiration. Here, we address this issue using in situ (14)C measurements of ecosystem respiration on an established peatland warming and vegetation manipulation experiment. Results show that warming of approximately 1 °C promotes respiration of ancient peatland carbon (up to 2100 years old) when dwarf-shrubs or graminoids are present, an effect not observed when only bryophytes are present. We demonstrate that warming likely promotes ancient peatland carbon release via its control over organic inputs from vascular plants. Our findings suggest that dwarf-shrubs and graminoids prime microbial decomposition of previously 'locked-up' organic matter from potentially deep in the peat profile, facilitating liberation of ancient carbon as CO2. Furthermore, such plant-induced peat respiration could contribute up to 40% of ecosystem CO2 emissions. If consistent across other subarctic and arctic ecosystems, this represents a considerable fraction of ecosystem respiration that is currently not acknowledged by global carbon cycle models. Ultimately, greater contribution of ancient carbon to ecosystem respiration may signal the loss of a previously stable peatland carbon pool, creating potential feedbacks to future climate change.

Vegetation exerts a greater control on litter decomposition than climate warming in peatlands.

Historically, slow decomposition rates have resulted in the accumulation of large amounts of carbon in northern peatlands. Both climate warming and vegetation change can alter rates of decomposition, and hence affect rates of atmospheric CO2 exchange, with consequences for climate change feedbacks. Although warming and vegetation change are happening concurrently, little is known about their relative and interactive effects on decomposition processes. To test the effects of warming and vegetation change on decomposition rates, we placed litter of three dominant species (Calluna vulgaris, Eriophorum vaginatum, Hypnum jutlandicum) into a peatland field experiment that combined warming.with plant functional group removals, and measured mass loss over two years. To identify potential mechanisms behind effects, we also measured nutrient cycling and soil biota. We found that plant functional group removals exerted a stronger control over short-term litter decomposition than did approximately 1 degrees C warming, and that the plant removal effect depended on litter species identity. Specifically, rates of litter decomposition were faster when shrubs were removed from the plant community, and these effects were strongest for graminoid and bryophyte litter. Plant functional group removals also had strong effects on soil biota and nutrient cycling associated with decomposition, whereby shrub removal had cascading effects on soil fungal community composition, increased enchytraeid abundance, and increased rates of N mineralization. Our findings demonstrate that, in addition to litter quality, changes in vegetation composition play a significant role in regulating short-term litter decomposition and belowground communities in peatland, and that these impacts can be greater than moderate warming effects. Our findings, albeit from a relatively short-term study, highlight the need to consider both vegetation change and its impacts below ground alongside climatic effects when predicting future decomposition rates and carbon storage in peatlands.

Contrasting growth responses of dominant peatland plants to warming and vegetation composition.

There is growing recognition that changes in vegetation composition can strongly influence peatland carbon cycling, with potential feedbacks to future climate. Nevertheless, despite accelerated climate and vegetation change in this ecosystem, the growth responses of peatland plant species to combined warming and vegetation change are unknown. Here, we used a field warming and vegetation removal experiment to test the hypothesis that dominant species from the three plant functional types present (dwarf-shrubs: Calluna vulgaris; graminoids: Eriophorum vaginatum; bryophytes: Sphagnum capillifolium) contrast in their growth responses to warming and the presence or absence of other plant functional types. Warming was accomplished using open top chambers, which raised air temperature by approximately 0.35 °C, and we measured air and soil microclimate as potential mechanisms through which both experimental factors could influence growth. We found that only Calluna growth increased with experimental warming (by 20%), whereas the presence of dwarf-shrubs and bryophytes increased growth of Sphagnum (46%) and Eriophorum (20%), respectively. Sphagnum growth was also negatively related to soil temperature, which was lower when dwarf-shrubs were present. Dwarf-shrubs may therefore promote Sphagnum growth by cooling the peat surface. Conversely, the effect of bryophyte presence on Eriophorum growth was not related to any change in microclimate, suggesting other factors play a role. In conclusion, our findings reveal contrasting abiotic and biotic controls over dominant peatland plant growth, suggesting that community composition and carbon cycling could be modified by simultaneous climate and vegetation change.

Interactive biotic and abiotic regulators of soil carbon cycling: evidence from controlled climate experiments on peatland and boreal soils.

Partially decomposed plant and animal remains have been accumulating in organic soils (i.e. >40% C content) for millennia, making them the largest terrestrial carbon store. There is growing concern that, in a warming world, soil biotic processing will accelerate and release greenhouse gases that further exacerbate climate change. However, the magnitude of this response remains uncertain as the constraints are abiotic, biotic and interactive. Here, we examined the influence of resource quality and biological activity on the temperature sensitivity of soil respiration under different soil moisture regimes. Organic soils were sampled from 13 boreal and peatland ecosystems located in the United Kingdom, Ireland, Spain, Finland and Sweden, representing a natural resource quality range of C, N and P. They were incubated at four temperatures (4, 10, 15 and 20 °C) at either 60% or 100% water holding capacity (WHC). Our results showed that chemical and biological properties play an important role in determining soil respiration responses to temperature and moisture changes. High soil C : P and C : N ratios were symptomatic of slow C turnover and long-term C accumulation. In boreal soils, low bacterial to fungal ratios were related to greater temperature sensitivity of respiration, which was amplified in drier conditions. This contrasted with peatland soils which were dominated by bacterial communities and enchytraeid grazing, resulting in a more rapid C turnover under warmer and wetter conditions. The unexpected acceleration of C mineralization under high moisture contents was possibly linked to the primarily role of fermented organic matter, instead of oxygen, in mediating microbial decomposition. We conclude that to improve C model simulations of soil respiration, a better resolution of the interactions occurring between climate, resource quality and the decomposer community will be required.

Wind farm and solar park effects on plant-soil carbon cycling: uncertain impacts of changes in ground-level microclimate.

Global energy demand is increasing as greenhouse gas driven climate change progresses, making renewable energy sources critical to future sustainable power provision. Land-based wind and solar electricity generation technologies are rapidly expanding, yet our understanding of their operational effects on biological carbon cycling in hosting ecosystems is limited. Wind turbines and photovoltaic panels can significantly change local ground-level climate by a magnitude that could affect the fundamental plant-soil processes that govern carbon dynamics. We believe that understanding the possible effects of changes in ground-level microclimates on these phenomena is crucial to reducing uncertainty of the true renewable energy carbon cost and to maximize beneficial effects. In this Opinions article, we examine the potential for the microclimatic effects of these land-based renewable energy sources to alter plant-soil carbon cycling, hypothesize likely effects and identify critical knowledge gaps for future carbon research.

Warming effects on greenhouse gas fluxes in peatlands are modulated by vegetation composition.

Understanding the effects of warming on greenhouse gas feedbacks to climate change represents a major global challenge. Most research has focused on direct effects of warming, without considering how concurrent changes in plant communities may alter such effects. Here, we combined vegetation manipulations with warming to investigate their interactive effects on greenhouse gas emissions from peatland. We found that although warming consistently increased respiration, the effect on net ecosystem CO2 exchange depended on vegetation composition. The greatest increase in CO2 sink strength after warming was when shrubs were present, and the greatest decrease when graminoids were present. CH4 was more strongly controlled by vegetation composition than by warming, with largest emissions from graminoid communities. Our results show that plant community composition is a significant modulator of greenhouse gas emissions and their response to warming, and suggest that vegetation change could alter peatland carbon sink strength under future climate change.

Microbial contributions to climate change through carbon cycle feedbacks.

There is considerable interest in understanding the biological mechanisms that regulate carbon exchanges between the land and atmosphere, and how these exchanges respond to climate change. An understanding of soil microbial ecology is central to our ability to assess terrestrial carbon cycle-climate feedbacks, but the complexity of the soil microbial community and the many ways that it can be affected by climate and other global changes hampers our ability to draw firm conclusions on this topic. In this paper, we argue that to understand the potential negative and positive contributions of soil microbes to land-atmosphere carbon exchange and global warming requires explicit consideration of both direct and indirect impacts of climate change on microorganisms. Moreover, we argue that this requires consideration of complex interactions and feedbacks that occur between microbes, plants and their physical environment in the context of climate change, and the influence of other global changes which have the capacity to amplify climate-driven effects on soil microbes. Overall, we emphasize the urgent need for greater understanding of how soil microbial ecology contributes to land-atmosphere carbon exchange in the context of climate change, and identify some challenges for the future. In particular, we highlight the need for a multifactor experimental approach to understand how soil microbes and their activities respond to climate change and consequences for carbon cycle feedbacks.