Climate change disrupts the seasonal coupling of plant and soil microbial nutrient cycling in an alpine ecosystem.

The seasonal coupling of plant and soil microbial nutrient demands is crucial for efficient ecosystem nutrient cycling and plant production, especially in strongly seasonal alpine ecosystems. Yet, how these seasonal nutrient cycling processes are modified by climate change and what the consequences are for nutrient loss and retention in alpine ecosystems remain unclear. Here, we explored how two pervasive climate change factors, reduced snow cover and shrub expansion, interactively modify the seasonal coupling of plant and soil microbial nitrogen (N) cycling in alpine grasslands, which are warming at double the rate of the global average. We found that the combination of reduced snow cover and shrub expansion disrupted the seasonal coupling of plant and soil N-cycling, with pronounced effects in spring (shortly after snow melt) and autumn (at the onset of plant senescence). In combination, both climate change factors decreased plant organic N-uptake by 70% and 82%, soil microbial biomass N by 19% and 38% and increased soil denitrifier abundances by 253% and 136% in spring and autumn, respectively. Shrub expansion also individually modified the seasonality of soil microbial community composition and stoichiometry towards more N-limited conditions and slower nutrient cycling in spring and autumn. In winter, snow removal markedly reduced the fungal:bacterial biomass ratio, soil N pools and shifted bacterial community composition. Taken together, our findings suggest that interactions between climate change factors can disrupt the temporal coupling of plant and soil microbial N-cycling processes in alpine grasslands. This could diminish the capacity of these globally widespread alpine ecosystems to retain N and support plant productivity under future climate change.

Deforestation impacts soil biodiversity and ecosystem services worldwide.

Deforestation poses a global threat to biodiversity and its capacity to deliver ecosystem services. Yet, the impacts of deforestation on soil biodiversity and its associated ecosystem services remain virtually unknown. We generated a global dataset including 696 paired-site observations to investigate how native forest conversion to other land uses affects soil properties, biodiversity, and functions associated with the delivery of multiple ecosystem services. The conversion of native forests to plantations, grasslands, and croplands resulted in higher bacterial diversity and more homogeneous fungal communities dominated by pathogens and with a lower abundance of symbionts. Such conversions also resulted in significant reductions in carbon storage, nutrient cycling, and soil functional rates related to organic matter decomposition. Responses of the microbial community to deforestation, including bacterial and fungal diversity and fungal guilds, were predominantly regulated by changes in soil pH and total phosphorus. Moreover, we found that soil fungal diversity and functioning in warmer and wetter native forests is especially vulnerable to deforestation. Our work highlights that the loss of native forests to managed ecosystems poses a major global threat to the biodiversity and functioning of soils and their capacity to deliver ecosystem services.

Cessation of grazing causes biodiversity loss and homogenization of soil food webs.

There is widespread concern that cessation of grazing in historically grazed ecosystems is causing biotic homogenization and biodiversity loss. We used 12 montane grassland sites along an 800 km north-south gradient across the UK, to test whether cessation of grazing affects local α- and ß-diversity of below-ground food webs. We show cessation of grazing leads to strongly decreased α-diversity of most groups of soil microbes and fauna, particularly of relatively rare taxa. By contrast, the ß-diversity varied between groups of soil organisms. While most soil microbial communities exhibited increased homogenization after cessation of grazing, we observed decreased homogenization for soil fauna after cessation of grazing. Overall, our results indicate that exclusion of domesticated herbivores from historically grazed montane grasslands has far-ranging negative consequences for diversity of below-ground food webs. This underscores the importance of grazers for maintaining the diversity of below-ground communities, which play a central role in ecosystem functioning.

Vegetation type, not the legacy of warming, modifies the response of microbial functional genes and greenhouse gas fluxes to drought in Oro-Arctic and alpine regions.

Climate warming and summer droughts alter soil microbial activity, affecting greenhouse gas (GHG) emissions in Arctic and alpine regions. However, the long-term effects of warming, and implications for future microbial resilience, are poorly understood. Using one alpine and three Arctic soils subjected to in situ long-term experimental warming, we simulated drought in laboratory incubations to test how microbial functional-gene abundance affects fluxes in three GHGs: carbon dioxide, methane, and nitrous oxide. We found that responses of functional gene abundances to drought and warming are strongly associated with vegetation type and soil carbon. Our sites ranged from a wet, forb dominated, soil carbon-rich systems to a drier, soil carbon-poor alpine site. Resilience of functional gene abundances, and in turn methane and carbon dioxide fluxes, was lower in the wetter, carbon-rich systems. However, we did not detect an effect of drought or warming on nitrous oxide fluxes. All gene-GHG relationships were modified by vegetation type, with stronger effects being observed in wetter, forb-rich soils. These results suggest that impacts of warming and drought on GHG emissions are linked to a complex set of microbial gene abundances and may be habitat-specific.

High intensity perturbations induce an abrupt shift in soil microbial state.

Soil microbial communities play a pivotal role in regulating ecosystem functioning. But they are increasingly being shaped by human-induced environmental change, including intense "pulse" perturbations, such as droughts, which are predicted to increase in frequency and intensity with climate change. While it is known that soil microbial communities are sensitive to such perturbations and that effects can be long-lasting, it remains untested whether there is a threshold in the intensity and frequency of perturbations that can trigger abrupt and persistent transitions in the taxonomic and functional characteristics of soil microbial communities. Here we demonstrate experimentally that intense pulses of drought equivalent to a 30-year drought event (<15% WHC) induce a major shift in the soil microbial community characterised by significantly altered bacterial and fungal community structures of reduced complexity and functionality. Moreover, the characteristics of this transformed microbial community persisted after returning soil to its previous moisture status. As a result, we found that drought had a strong legacy effect on bacterial community function, inducing an enhanced growth rate following subsequent drought. Abrupt transitions are widely documented in aquatic and terrestrial plant communities in response to human-induced perturbations. Our findings demonstrate that such transitions also occur in soil microbial communities in response to high intensity pulse perturbations, with potentially deleterious consequences for soil health.

Leaf metabolic traits reveal hidden dimensions of plant form and function.

The metabolome is the biochemical basis of plant form and function, but we know little about its macroecological variation across the plant kingdom. Here, we used the plant functional trait concept to interpret leaf metabolome variation among 457 tropical and 339 temperate plant species. Distilling metabolite chemistry into five metabolic functional traits reveals that plants vary on two major axes of leaf metabolic specialization-a leaf chemical defense spectrum and an expression of leaf longevity. Axes are similar for tropical and temperate species, with many trait combinations being viable. However, metabolic traits vary orthogonally to life-history strategies described by widely used functional traits. The metabolome thus expands the functional trait concept by providing additional axes of metabolic specialization for examining plant form and function.

Soil biodiversity needs policy without borders.

Soil health laws should account for global soil connections.

Defoliation and fertilisation differentially moderate root trait effects on soil abiotic and biotic properties.

Root functional traits are known to influence soil properties that underpin ecosystem functioning. Yet few studies have explored how root traits simultaneously influence physical, chemical, and biological properties of soil, or how these responses are modified by common grassland perturbations that shape roots, such as defoliation and fertilisation.Here, we explored how root traits of a wide range of grassland plant species with contrasting resource acquisition strategies (i.e. conservative vs. exploitative strategy plant species) respond to defoliation and fertilisation individually and in combination, and examined cascading impacts on a range of soil abiotic and biotic properties that underpin ecosystem functioning.We found that the amplitude of the response of root traits to defoliation and fertilisation varied among plant species, in most cases independently of plant resource acquisition strategies. However, the direction of the root trait responses (increase or decrease) to perturbations was consistent across all plant species, with defoliation and fertilisation exerting opposing effects on root traits. Specific root length increased relative to non-perturbed control in response to defoliation, while root biomass, root mass density, and root length density decreased. Fertilisation induced the opposite responses. We also found that both defoliation and fertilisation individually enhanced the role of root traits in regulating soil biotic and abiotic properties, especially soil aggregate stability. Synthesis: Our results indicate that defoliation and fertilisation, two common grassland perturbations, have contrasting impacts on root traits of grassland plant species, with direct and indirect short-term consequences for a wide range of soil abiotic and biotic properties that underpin ecosystem functioning.

Intensive grassland management disrupts below-ground multi-trophic resource transfer in response to drought.

Modification of soil food webs by land management may alter the response of ecosystem processes to climate extremes, but empirical support is limited and the mechanisms involved remain unclear. Here we quantify how grassland management modifies the transfer of recent photosynthates and soil nitrogen through plants and soil food webs during a post-drought period in a controlled field experiment, using in situ 13C and 15N pulse-labelling in intensively and extensively managed fields. We show that intensive management decrease plant carbon (C) capture and its transfer through components of food webs and soil respiration compared to extensive management. We observe a legacy effect of drought on C transfer pathways mainly in intensively managed grasslands, by increasing plant C assimilation and 13C released as soil CO2 efflux but decreasing its transfer to roots, bacteria and Collembola. Our work provides insight into the interactive effects of grassland management and drought on C transfer pathways, and highlights that capture and rapid transfer of photosynthates through multi-trophic networks are key for maintaining grassland resistance to drought.

Shrub expansion modulates belowground impacts of changing snow conditions in alpine grasslands.

Climate change is disproportionately impacting mountain ecosystems, leading to large reductions in winter snow cover, earlier spring snowmelt and widespread shrub expansion into alpine grasslands. Yet, the combined effects of shrub expansion and changing snow conditions on abiotic and biotic soil properties remains poorly understood. We used complementary field experiments to show that reduced snow cover and earlier snowmelt have effects on soil microbial communities and functioning that persist into summer. However, ericaceous shrub expansion modulates a number of these impacts and has stronger belowground effects than changing snow conditions. Ericaceous shrub expansion did not alter snow depth or snowmelt timing but did increase the abundance of ericoid mycorrhizal fungi and oligotrophic bacteria, which was linked to decreased soil respiration and nitrogen availability. Our findings suggest that changing winter snow conditions have cross-seasonal impacts on soil properties, but shifts in vegetation can modulate belowground effects of future alpine climate change.

Local stability properties of complex, species-rich soil food webs with functional block structure.

Ecologists have long debated the properties that confer stability to complex, species-rich ecological networks. Species-level soil food webs are large and structured networks of central importance to ecosystem functioning. Here, we conducted an analysis of the stability properties of an up-to-date set of theoretical soil food web models that account both for realistic levels of species richness and the most recent views on the topological structure (who is connected to whom) of these food webs. The stability of the network was best explained by two factors: strong correlations between interaction strengths and the blocked, nonrandom trophic structure of the web. These two factors could stabilize our model food webs even at the high levels of species richness that are typically found in soil, and that would make random systems very unstable. Also, the stability of our soil food webs is well-approximated by the cascade model. This result suggests that stability could emerge from the hierarchical structure of the functional organization of the web. Our study shows that under the assumption of equilibrium and small perturbations, theoretical soil food webs possess a topological structure that allows them to be complex yet more locally stable than their random counterpart. In particular, results strongly support the general hypothesis that the stability of rich and complex soil food webs is mostly driven by correlations in interaction strength and the organization of the soil food web into functional groups. The implication is that in real-world food web, any force disrupting the functional structure and distribution pattern of interaction strengths (i.e., energy fluxes) of the soil food webs will destabilize the dynamics of the system, leading to species extinction and major changes in the relative abundances of species.

Aridity-driven shift in biodiversity-soil multifunctionality relationships.

Relationships between biodiversity and multiple ecosystem functions (that is, ecosystem multifunctionality) are context-dependent. Both plant and soil microbial diversity have been reported to regulate ecosystem multifunctionality, but how their relative importance varies along environmental gradients remains poorly understood. Here, we relate plant and microbial diversity to soil multifunctionality across 130 dryland sites along a 4,000 km aridity gradient in northern China. Our results show a strong positive association between plant species richness and soil multifunctionality in less arid regions, whereas microbial diversity, in particular of fungi, is positively associated with multifunctionality in more arid regions. This shift in the relationships between plant or microbial diversity and soil multifunctionality occur at an aridity level of ∼0.8, the boundary between semiarid and arid climates, which is predicted to advance geographically ∼28% by the end of the current century. Our study highlights that biodiversity loss of plants and soil microorganisms may have especially strong consequences under low and high aridity conditions, respectively, which calls for climate-specific biodiversity conservation strategies to mitigate the effects of aridification.

Do soil depth and plant community composition interact to modify the resistance and resilience of grassland ecosystem functioning to drought?

While the effect of drought on plant communities and their associated ecosystem functions is well studied, little research has considered how responses are modified by soil depth and depth heterogeneity. We conducted a mesocosm study comprising shallow and deep soils, and variable and uniform soil depths, and two levels of plant community composition, and exposed them to a simulated drought to test for interactive effects of these treatments on the resilience of carbon dioxide fluxes, plant functional traits, and soil chemical properties. We tested the hypotheses that: (a) shallow and variable depth soils lead to increased resistance and resilience of ecosystem functions to drought due to more exploitative plant trait strategies; (b) plant communities associated with intensively managed high fertility soils, will have more exploitative root traits than extensively managed, lower fertility plant communities. These traits will be associated with higher resistance and resilience to drought and may interact with soil depth and depth heterogeneity to amplify the effects on ecosystem functions. Our results showed that while there were strong soil depth/heterogeneity effects on plant-driven carbon fluxes, it did not affect resistance or resilience to drought, and there were no treatment effects on plant-available carbon or nitrogen. We did observe a significant increase in exploitative root traits in shallow and variable soils relative to deep and uniform, which may have resulted in a compensation effect which led to the similar drought responses. Plant community compositions representative of intensive management were more drought resilient than more diverse "extensive" communities irrespective of soil depth or soil depth heterogeneity. In intensively managed plant communities, root traits were more representative of exploitative strategies. Taken together, our results suggest that reorganization of root traits in response to soil depth could buffer drought effects on ecosystem functions.

Reduced microbial stability in the active layer is associated with carbon loss under alpine permafrost degradation.

Permafrost degradation may induce soil carbon (C) loss, critical for global C cycling, and be mediated by microbes. Despite larger C stored within the active layer of permafrost regions, which are more affected by warming, and the critical roles of Qinghai-Tibet Plateau in C cycling, most previous studies focused on the permafrost layer and in high-latitude areas. We demonstrate in situ that permafrost degradation alters the diversity and potentially decreases the stability of active layer microbial communities. These changes are associated with soil C loss and potentially a positive C feedback. This study provides insights into microbial-mediated mechanisms responsible for C loss within the active layer in degraded permafrost, aiding in the modeling of C emission under future scenarios.

Contrasting responses of above- and belowground diversity to multiple components of land-use intensity.

Land-use intensification is a major driver of biodiversity loss. However, understanding how different components of land use drive biodiversity loss requires the investigation of multiple trophic levels across spatial scales. Using data from 150 agricultural grasslands in central Europe, we assess the influence of multiple components of local- and landscape-level land use on more than 4,000 above- and belowground taxa, spanning 20 trophic groups. Plot-level land-use intensity is strongly and negatively associated with aboveground trophic groups, but positively or not associated with belowground trophic groups. Meanwhile, both above- and belowground trophic groups respond to landscape-level land use, but to different drivers: aboveground diversity of grasslands is promoted by diverse surrounding land-cover, while belowground diversity is positively related to a high permanent forest cover in the surrounding landscape. These results highlight a role of landscape-level land use in shaping belowground communities, and suggest that revised agroecosystem management strategies are needed to conserve whole-ecosystem biodiversity.

Stoichiometric traits (N:P) of understory plants contribute to reductions in plant diversity following long-term nitrogen addition in subtropical forest.

Nitrogen enrichment is pervasive in forest ecosystems, but its influence on understory plant communities and their stoichiometric characteristics is poorly understood. We hypothesize that when forest is enriched with nitrogen (N), the stoichiometric characteristics of plant species explain changes in understory plant diversity. A 13-year field experiment was conducted to explore the effects of N addition on foliar carbon (C): N: phosphorus (P) stoichiometry, understory plant species richness, and intrinsic water use efficiency (iWUE) in a subtropical Chinese fir forest. Four levels of N addition were applied: 0, 6, 12, and 24 g m-2 year-1. Individual plant species were categorized into resistant plants, intermediate resistant plants, and sensitive plants based on their response to nitrogen addition. Results showed that N addition significantly decreased the number of species, genera, and families of herbaceous plants. Foliar N:P ratios were greater in sensitive plants than resistant or intermediate resistant plants, while iWUE showed an opposite trend. However, no relationship was detected between soil available N and foliar N, and soil N:P and foliar N:P ratios. Our results indicated that long-term N addition decreased the diversity of understory plants in a subtropical forest. Through regulating water use efficiency with N addition, sensitive plants change their N:P stoichiometry and have a higher risk of mortality, while resistant plants maintain a stable N:P stoichiometry, which contributes to their survival. These findings suggest that plant N:P stoichiometry plays an important role in understory plant performance in response to environmental change of N.

Climate change alters temporal dynamics of alpine soil microbial functioning and biogeochemical cycling via earlier snowmelt.

Soil microbial communities regulate global biogeochemical cycles and respond rapidly to changing environmental conditions. However, understanding how soil microbial communities respond to climate change, and how this influences biogeochemical cycles, remains a major challenge. This is especially pertinent in alpine regions where climate change is taking place at double the rate of the global average, with large reductions in snow cover and earlier spring snowmelt expected as a consequence. Here, we show that spring snowmelt triggers an abrupt transition in the composition of soil microbial communities of alpine grassland that is closely linked to shifts in soil microbial functioning and biogeochemical pools and fluxes. Further, by experimentally manipulating snow cover we show that this abrupt seasonal transition in wide-ranging microbial and biogeochemical soil properties is advanced by earlier snowmelt. Preceding winter conditions did not change the processes that take place during snowmelt. Our findings emphasise the importance of seasonal dynamics for soil microbial communities and the biogeochemical cycles that they regulate. Moreover, our findings suggest that earlier spring snowmelt due to climate change will have far reaching consequences for microbial communities and nutrient cycling in these globally widespread alpine ecosystems.

Soil microbial diversity-biomass relationships are driven by soil carbon content across global biomes.

The relationship between biodiversity and biomass has been a long standing debate in ecology. Soil biodiversity and biomass are essential drivers of ecosystem functions. However, unlike plant communities, little is known about how the diversity and biomass of soil microbial communities are interlinked across globally distributed biomes, and how variations in this relationship influence ecosystem function. To fill this knowledge gap, we conducted a field survey across global biomes, with contrasting vegetation and climate types. We show that soil carbon (C) content is associated to the microbial diversity-biomass relationship and ratio in soils across global biomes. This ratio provides an integrative index to identify those locations on Earth wherein diversity is much higher compared with biomass and vice versa. The soil microbial diversity-to-biomass ratio peaks in arid environments with low C content, and is very low in C-rich cold environments. Our study further advances that the reductions in soil C content associated with land use intensification and climate change could cause dramatic shifts in the microbial diversity-biomass ratio, with potential consequences for broad soil processes.