Mycorrhizal type and tree diversity affect foliar elemental pools and stoichiometry.

Species-specific differences in nutrient acquisition strategies allow for complementary use of resources among plants in mixtures, which may be further shaped by mycorrhizal associations. However, empirical evidence of this potential role of mycorrhizae is scarce, particularly for tree communities. We investigated the impact of tree species richness and mycorrhizal types, arbuscular mycorrhizal fungi (AM) and ectomycorrhizal fungi (EM), on above- and belowground carbon (C), nitrogen (N), and phosphorus (P) dynamics. Soil and soil microbial biomass elemental dynamics showed weak responses to tree species richness and none to mycorrhizal type. However, foliar elemental concentrations, stoichiometry, and pools were significantly affected by both treatments. Tree species richness increased foliar C and P pools but not N pools. Additive partitioning analyses showed that net biodiversity effects of foliar C, N, P pools in EM tree communities were driven by selection effects, but in mixtures of both mycorrhizal types by complementarity effects. Furthermore, increased tree species richness reduced soil nitrate availability, over 2 yr. Our results indicate that positive effects of tree diversity on aboveground nutrient storage are mediated by complementary mycorrhizal strategies and highlight the importance of using mixtures composed of tree species with different types of mycorrhizae to achieve more multifunctional afforestation.

Stronger compensatory thermal adaptation of soil microbial respiration with higher substrate availability.

Ongoing global warming is expected to augment soil respiration by increasing the microbial activity, driving self-reinforcing feedback to climate change. However, the compensatory thermal adaptation of soil microorganisms and substrate depletion may weaken the effects of rising temperature on soil respiration. To test this hypothesis, we collected soils along a large-scale forest transect in eastern China spanning a natural temperature gradient, and we incubated the soils at different temperatures with or without substrate addition. We combined the exponential thermal response function and a data-driven model to study the interaction effect of thermal adaptation and substrate availability on microbial respiration and compared our results to those from two additional continental and global independent datasets. Modeled results suggested that the effect of thermal adaptation on microbial respiration was greater in areas with higher mean annual temperatures, which is consistent with the compensatory response to warming. In addition, the effect of thermal adaptation on microbial respiration was greater under substrate addition than under substrate depletion, which was also true for the independent datasets reanalyzed using our approach. Our results indicate that thermal adaptation in warmer regions could exert a more pronounced negative impact on microbial respiration when the substrate availability is abundant. These findings improve the body of knowledge on how substrate availability influences the soil microbial community-temperature interactions, which could improve estimates of projected soil carbon losses to the atmosphere through respiration.

Self-organization as a mechanism of resilience in dryland ecosystems.

Self-organized spatial patterns are a common feature of complex systems, ranging from microbial communities to mussel beds and drylands. While the theoretical implications of these patterns for ecosystem-level processes, such as functioning and resilience, have been extensively studied, empirical evidence remains scarce. To address this gap, we analyzed global drylands along an aridity gradient using remote sensing, field data, and modeling. We found that the spatial structure of the vegetation strengthens as aridity increases, which is associated with the maintenance of a high level of soil multifunctionality, even as aridity levels rise up to a certain threshold. The combination of these results with those of two individual-based models indicate that self-organized vegetation patterns not only form in response to stressful environmental conditions but also provide drylands with the ability to adapt to changing conditions while maintaining their functioning, an adaptive capacity which is lost in degraded ecosystems. Self-organization thereby plays a vital role in enhancing the resilience of drylands. Overall, our findings contribute to a deeper understanding of the relationship between spatial vegetation patterns and dryland resilience. They also represent a significant step forward in the development of indicators for ecosystem resilience, which are critical tools for managing and preserving these valuable ecosystems in a warmer and more arid world.

Biotic homogenization, lower soil fungal diversity and fewer rare taxa in arable soils across Europe.

Soil fungi are a key constituent of global biodiversity and play a pivotal role in agroecosystems. How arable farming affects soil fungal biogeography and whether it has a disproportional impact on rare taxa is poorly understood. Here, we used the high-resolution PacBio Sequel targeting the entire ITS region to investigate the distribution of soil fungi in 217 sites across a 3000 km gradient in Europe. We found a consistently lower diversity of fungi in arable lands than grasslands, with geographic locations significantly impacting fungal community structures. Prevalent fungal groups became even more abundant, whereas rare groups became fewer or absent in arable lands, suggesting a biotic homogenization due to arable farming. The rare fungal groups were narrowly distributed and more common in grasslands. Our findings suggest that rare soil fungi are disproportionally affected by arable farming, and sustainable farming practices should protect rare taxa and the ecosystem services they support.

Extreme drought impacts have been underestimated in grasslands and shrublands globally.

Climate change is increasing the frequency and severity of short-term (~1 y) drought events-the most common duration of drought-globally. Yet the impact of this intensification of drought on ecosystem functioning remains poorly resolved. This is due in part to the widely disparate approaches ecologists have employed to study drought, variation in the severity and duration of drought studied, and differences among ecosystems in vegetation, edaphic and climatic attributes that can mediate drought impacts. To overcome these problems and better identify the factors that modulate drought responses, we used a coordinated distributed experiment to quantify the impact of short-term drought on grassland and shrubland ecosystems. With a standardized approach, we imposed ~a single year of drought at 100 sites on six continents. Here we show that loss of a foundational ecosystem function-aboveground net primary production (ANPP)-was 60% greater at sites that experienced statistically extreme drought (1-in-100-y event) vs. those sites where drought was nominal (historically more common) in magnitude (35% vs. 21%, respectively). This reduction in a key carbon cycle process with a single year of extreme drought greatly exceeds previously reported losses for grasslands and shrublands. Our global experiment also revealed high variability in drought response but that relative reductions in ANPP were greater in drier ecosystems and those with fewer plant species. Overall, our results demonstrate with unprecedented rigor that the global impacts of projected increases in drought severity have been significantly underestimated and that drier and less diverse sites are likely to be most vulnerable to extreme drought.

Connecting the multiple dimensions of global soil fungal diversity.

How the multiple facets of soil fungal diversity vary worldwide remains virtually unknown, hindering the management of this essential species-rich group. By sequencing high-resolution DNA markers in over 4000 topsoil samples from natural and human-altered ecosystems across all continents, we illustrate the distributions and drivers of different levels of taxonomic and phylogenetic diversity of fungi and their ecological groups. We show the impact of precipitation and temperature interactions on local fungal species richness (alpha diversity) across different climates. Our findings reveal how temperature drives fungal compositional turnover (beta diversity) and phylogenetic diversity, linking them with regional species richness (gamma diversity). We integrate fungi into the principles of global biodiversity distribution and present detailed maps for biodiversity conservation and modeling of global ecological processes.

Nitrogen addition delays the emergence of an aridity-induced threshold for plant biomass.

Crossing certain aridity thresholds in global drylands can lead to abrupt decays of ecosystem attributes such as plant productivity, potentially causing land degradation and desertification. It is largely unknown, however, whether these thresholds can be altered by other key global change drivers known to affect the water-use efficiency and productivity of vegetation, such as elevated CO2 and nitrogen (N). Using >5000 empirical measurements of plant biomass, we showed that crossing an aridity (1-precipitation/potential evapotranspiration) threshold of ∼0.50, which marks the transition from dry sub-humid to semi-arid climates, led to abrupt declines in aboveground biomass (AGB) and progressive increases in root:shoot ratios, thus importantly affecting carbon stocks and their distribution. N addition significantly increased AGB and delayed the emergence of its aridity threshold from 0.49 to 0.55 (P < 0.05). By coupling remote sensing estimates of leaf area index with simulations from multiple models, we found that CO2 enrichment did not alter the observed aridity threshold. By 2100, and under the RCP 8.5 scenario, we forecast a 0.3% net increase in the global land area exceeding the aridity threshold detected under a scenario that includes N deposition, in comparison to a 2.9% net increase if the N effect is not considered. Our study thus indicates that N addition could mitigate to a great extent the negative impact of increasing aridity on plant biomass in drylands. These findings are critical for improving forecasts of abrupt vegetation changes in response to ongoing global environmental change.

The global biogeography and environmental drivers of fairy circles.

Fairy circles (FCs) are regular vegetation patterns found in drylands of Namibia and Western Australia. It is virtually unknown whether they are also present in other regions of the world and which environmental factors determine their distribution. We conducted a global systematic survey and found FC-like vegetation patterns in 263 sites from 15 countries and three continents, including the Sahel, Madagascar, and Middle-West Asia. FC-like vegetation patterns are found in environments characterized by a unique combination of soil (including low nutrient levels and high sand content) and climatic (arid regions with high temperatures and high precipitation seasonality) conditions. In addition to these factors, the presence of specific biological elements (termite nests) in certain regions also plays a role in the presence of these patterns. Furthermore, areas with FC-like vegetation patterns also showed more stable temporal productivity patterns than those of surrounding areas. Our study presents a global atlas of FCs and provides unique insights into the ecology and biogeography of these fascinating vegetation patterns.

Symbiotic status alters fungal eco-evolutionary offspring trajectories.

Despite host-fungal symbiotic interactions being ubiquitous in all ecosystems, understanding how symbiosis has shaped the ecology and evolution of fungal spores that are involved in dispersal and colonization of their hosts has been ignored in life-history studies. We assembled a spore morphology database covering over 26,000 species of free-living to symbiotic fungi of plants, insects and humans and found more than eight orders of variation in spore size. Evolutionary transitions in symbiotic status correlated with shifts in spore size, but the strength of this effect varied widely among phyla. Symbiotic status explained more variation than climatic variables in the current distribution of spore sizes of plant-associated fungi at a global scale while the dispersal potential of their spores is more restricted compared to free-living fungi. Our work advances life-history theory by highlighting how the interaction between symbiosis and offspring morphology shapes the reproductive and dispersal strategies among living forms.

Water availability creates global thresholds in multidimensional soil biodiversity and functions.

Soils support an immense portion of Earth's biodiversity and maintain multiple ecosystem functions which are essential for human well-being. Environmental thresholds are known to govern global vegetation patterns, but it is still unknown whether they can be used to predict the distribution of soil organisms and functions across global biomes. Using a global field survey of 383 sites across contrasting climatic and vegetation conditions, here we showed that soil biodiversity and functions exhibited pervasive nonlinear patterns worldwide and are mainly governed by water availability (precipitation and potential evapotranspiration). Changes in water availability resulted in drastic shifts in soil biodiversity (bacteria, fungi, protists and invertebrates) and soil functions including plant-microbe interactions, plant productivity, soil biogeochemical cycles and soil carbon sequestration. Our findings highlight that crossing specific water availability thresholds can have critical consequences for the provision of essential ecosystem services needed to sustain our planet.

Biocrusts Modulate Climate Change Effects on Soil Organic Carbon Pools: Insights From a 9-Year Experiment.

Accumulating evidence suggests that warming associated with climate change is decreasing the total amount of soil organic carbon (SOC) in drylands, although scientific research has not given enough emphasis to particulate (POC) and mineral-associated organic carbon (MAOC) pools. Biocrusts are a major biotic feature of drylands and have large impacts on the C cycle, yet it is largely unknown whether they modulate the responses of POC and MAOC to climate change. Here, we assessed the effects of simulated climate change (control, reduced rainfall (RE), warming (WA), and RE + WA) and initial biocrust cover (low (< 20%) versus high (> 50%)) on the mineral protection of soil C and soil organic matter quality in a dryland ecosystem in central Spain for 9 years. At low initial biocrust cover levels, both WA and RE + WA increased SOC, especially POC but also MAOC, and promoted a higher contribution of carbohydrates, relative to aromatic compounds, to the POC fraction. These results suggest that the accumulation of soil C under warming treatments may be transitory in soils with low initial biocrust cover. In soils with high initial biocrust cover, climate change treatments did not affect SOC, neither POC nor MAOC fraction. Overall, our results indicate that biocrust communities modulate the negative effect of climate change on SOC, because no losses of soil C were observed with the climate manipulations under biocrusts. Future work should focus on determining the long-term persistence of the observed buffering effect by biocrust-forming lichens, as they are known to be negatively affected by warming. Supplementary Information: The online version contains supplementary material available at 10.1007/s10021-022-00779-0.

The impact of agricultural management on soil aggregation and carbon storage is regulated by climatic thresholds across a 3000 km European gradient.

Organic carbon and aggregate stability are key features of soil quality and are important to consider when evaluating the potential of agricultural soils as carbon sinks. However, we lack a comprehensive understanding of how soil organic carbon (SOC) and aggregate stability respond to agricultural management across wide environmental gradients. Here, we assessed the impact of climatic factors, soil properties and agricultural management (including land use, crop cover, crop diversity, organic fertilization, and management intensity) on SOC and the mean weight diameter of soil aggregates, commonly used as an indicator for soil aggregate stability, across a 3000 km European gradient. Soil aggregate stability (-56%) and SOC stocks (-35%) in the topsoil (20 cm) were lower in croplands compared with neighboring grassland sites (uncropped sites with perennial vegetation and little or no external inputs). Land use and aridity were strong drivers of soil aggregation explaining 33% and 20% of the variation, respectively. SOC stocks were best explained by calcium content (20% of explained variation) followed by aridity (15%) and mean annual temperature (10%). We also found a threshold-like pattern for SOC stocks and aggregate stability in response to aridity, with lower values at sites with higher aridity. The impact of crop management on aggregate stability and SOC stocks appeared to be regulated by these thresholds, with more pronounced positive effects of crop diversity and more severe negative effects of crop management intensity in nondryland compared with dryland regions. We link the higher sensitivity of SOC stocks and aggregate stability in nondryland regions to a higher climatic potential for aggregate-mediated SOC stabilization. The presented findings are relevant for improving predictions of management effects on soil structure and C storage and highlight the need for site-specific agri-environmental policies to improve soil quality and C sequestration.

Continuous monitoring of chlorophyll a fluorescence and microclimatic conditions reveals warming-induced physiological damage in biocrust-forming lichens.

Purpose: Biocrust communities, which are important regulators of multiple ecosystem functions in drylands, are highly sensitive to climate change. There is growing evidence of the negative impacts of warming on the performance of biocrust constituents like lichens in the field. Here, we aim to understand the physiological basis behind this pattern. Methods: Using a unique manipulative climate change experiment, we monitored every 30 minutes and for 9 months the chlorophyll a fluorescence and microclimatic conditions (lichen surface temperature, relative moisture and photosynthetically active radiation) of Psora decipiens, a key biocrust constituent in drylands worldwide. This long-term monitoring resulted in 11,847 records at the thallus-level, which allowed us to evaluate the impacts of ~2.3 °C simulated warming treatment on the physiology of Psora at an unprecedented level of detail. Results: Simulated warming and the associated decrease in relative moisture promoted by this treatment negatively impacted the physiology of Psora, especially during the diurnal period of the spring, when conditions are warmer and drier. These impacts were driven by a mechanism based on the reduction of the length of the periods allowing net photosynthesis, and by declines in Yield and Fv/Fm under simulated warming. Conclusion: Our study reveals the physiological basis explaining observed negative impacts of ongoing global warming on biocrust-forming lichens in the field. The functional response observed could limit the growth and cover of biocrust-forming lichens in drylands in the long-term, negatively impacting in key soil attributes such as biogeochemical cycles, water balance, biological activity and ability of controlling erosion. Supplementary Information: The online version contains supplementary material available at 10.1007/s11104-022-05686-w.

Drylands contribute disproportionately to observed global productivity increases.

Drylands cover about 40% of the terrestrial surface and are sensitive to climate change, but their relative contributions to global vegetation greening and productivity increase in recent decades are still poorly known. Here, by integrating satellite data and biosphere modeling, we showed that drylands contributed more to global gross primary productivity (GPP) increase (65% ± 16%) than to Earth greening (33% ± 15%) observed during 1982-2015. The enhanced productivity per unit leaf area, i.e., light-use efficiency (LUE), was the mechanism behind this pattern. We also found that LUE was more sensitive to soil moisture than to atmospheric vapor pressure deficit (VPD) in drylands, while the opposite was observed (i.e., LUE was more sensitive to VPD) in humid areas. Our findings suggest the importance of using different moisture stress metrics in projecting the vegetation productivity changes of dry versus humid regions and highlight the prominent role of drylands as key controllers of the global carbon cycle.

Soils in warmer and less developed countries have less micronutrients globally.

Soil micronutrients are capital for the delivery of ecosystem functioning and food provision worldwide. Yet, despite their importance, the global biogeography and ecological drivers of soil micronutrients remain virtually unknown, limiting our capacity to anticipate abrupt unexpected changes in soil micronutrients in the face of climate change. Here, we analyzed >1300 topsoil samples to examine the global distribution of six metallic micronutrients (Cu, Fe, Mn, Zn, Co and Ni) across all continents, climates and vegetation types. We found that warmer arid and tropical ecosystems, present in the least developed countries, sustain the lowest contents of multiple soil micronutrients. We further provide evidence that temperature increases may potentially result in abrupt and simultaneous reductions in the content of multiple soil micronutrients when a temperature threshold of 12-14°C is crossed, which may be occurring on 3% of the planet over the next century. Altogether, our findings provide fundamental understanding of the global distribution of soil micronutrients, with direct implications for the maintenance of ecosystem functioning, rangeland management and food production in the warmest and poorest regions of the planet.

The global distribution and environmental drivers of the soil antibiotic resistome.

BACKGROUND: Little is known about the global distribution and environmental drivers of key microbial functional traits such as antibiotic resistance genes (ARGs). Soils are one of Earth's largest reservoirs of ARGs, which are integral for soil microbial competition, and have potential implications for plant and human health. Yet, their diversity and global patterns remain poorly described. Here, we analyzed 285 ARGs in soils from 1012 sites across all continents and created the first global atlas with the distributions of topsoil ARGs. RESULTS: We show that ARGs peaked in high latitude cold and boreal forests. Climatic seasonality and mobile genetic elements, associated with the transmission of antibiotic resistance, were also key drivers of their global distribution. Dominant ARGs were mainly related to multidrug resistance genes and efflux pump machineries. We further pinpointed the global hotspots of the diversity and proportions of soil ARGs. CONCLUSIONS: Together, our work provides the foundation for a better understanding of the ecology and global distribution of the environmental soil antibiotic resistome. Video Abstract.

Grazing and ecosystem service delivery in global drylands.

Grazing represents the most extensive use of land worldwide. Yet its impacts on ecosystem services remain uncertain because pervasive interactions between grazing pressure, climate, soil properties, and biodiversity may occur but have never been addressed simultaneously. Using a standardized survey at 98 sites across six continents, we show that interactions between grazing pressure, climate, soil, and biodiversity are critical to explain the delivery of fundamental ecosystem services across drylands worldwide. Increasing grazing pressure reduced ecosystem service delivery in warmer and species-poor drylands, whereas positive effects of grazing were observed in colder and species-rich areas. Considering interactions between grazing and local abiotic and biotic factors is key for understanding the fate of dryland ecosystems under climate change and increasing human pressure.

Biocrusts increase the resistance to warming-induced increases in topsoil P pools.

Ongoing global warming and alterations in rainfall patterns driven by climate change are known to have large impacts on biogeochemical cycles, particularly on drylands. In addition, the global increase in atmospheric nitrogen (N) deposition can destabilize primary productivity in terrestrial ecosystems, and phosphorus (P) may become the most limiting nutrient in many terrestrial ecosystems. However, the impacts of climate change on soil P pools in drylands remain poorly understood. Furthermore, it is unknown whether biocrusts, a major biotic component of drylands worldwide, modulate such impacts.Here we used two long-term (8-10 years) experiments conducted in Central (Aranjuez) and SE (Sorbas) Spain to test how a ~2.5°C warming, a ~30% rainfall reduction and biocrust cover affected topsoil (0-1 cm) P pools (non-occluded P, organic P, calcium bound P, occluded P and total P).Warming significantly increased most P pools-except occluded P-in Aranjuez, whereas only augmented non-occluded P in Sorbas. The rainfall reduction treatment had no effect on the soil P pools at any experimental site. Biocrusts increased most soil P pools and conferred resistance to simulated warming for major P pools at both sites, and to rainfall reduction for non-occluded and occluded P in Aranjuez. Synthesis. Our findings provide novel insights on the responses of soil P pools to warming and rainfall reduction, and highlight the importance of biocrusts as modulators of these responses in dryland ecosystems. Our results suggest that the observed negative impacts of warming on dryland biocrust communities will decrease their capacity to buffer changes in topsoil P driven by climate change.

Tanto el calentamiento global en curso como las alteraciones en los patrones de precipitaciones provocados por el cambio climático tienen grandes impactos en los ciclos biogeoquímicos, particularmente en los ecosistemas áridos y semiáridos. Además, el aumento global de la deposición de nitrógeno (N) atmosférico puede desestabilizar la productividad primaria en los ecosistemas terrestres, y el fósforo (P) puede convertirse en el nutriente más limitante en muchos de estos ecosistemas. Sin embargo, los impactos del cambio climático en las reservas de P del suelo en los ecosistemas áridos y semiáridos siguen sin comprenderse totalmente. Además, se desconoce si la costra biológica del suelo, un componente biótico importante de los ecosistemas áridos y semiáridos en todo el mundo, modulan tales impactos.Utilizamos dos experimentos a largo plazo (8­10 años) ubicados en el centro (Aranjuez) y el sureste (Sorbas) de España para probar cómo el calentamiento de ~2,5°C, la reducción de las precipitaciones de ~30 % y la cobertura de costra biológica afectaron los pools de P (P no ocluido, P orgánico, P ligado al calcio, P ocluido y P total) de la capa superior del suelo (0­1 cm).El calentamiento aumentó significativamente la mayoría de los pools de P ­excepto el P ocluido­ en Aranjuez, mientras que solo aumentó el P no ocluido en Sorbas. El tratamiento de reducción de las precipitaciones no tuvo efecto en los pools de P del suelo en ningún sitio experimental. La costra biológica aumentó la mayoría de los depósitos de P del suelo y confirieron resistencia al calentamiento simulado para los principales pools de P en ambos sitios, y a la reducción de las precipitaciones para el P no ocluido y ocluido en Aranjuez. Síntesis. Nuestros hallazgos brindan información novedosa sobre las respuestas de los pools de P del suelo al calentamiento y la reducción de las precipitaciones, y resaltan la importancia de la costra biológica como moduladora de estas respuestas en los ecosistemas áridos y semiáridos. Nuestros resultados sugieren que los impactos negativos observados del calentamiento en las comunidades de costra biológica de los ecosistemas áridos y semiáridos disminuirán su capacidad para amortiguar los cambios en el P del suelo provocados por el cambio climático.

Global patterns in endemicity and vulnerability of soil fungi.

Fungi are highly diverse organisms, which provide multiple ecosystem services. However, compared with charismatic animals and plants, the distribution patterns and conservation needs of fungi have been little explored. Here, we examined endemicity patterns, global change vulnerability and conservation priority areas for functional groups of soil fungi based on six global surveys using a high-resolution, long-read metabarcoding approach. We found that the endemicity of all fungi and most functional groups peaks in tropical habitats, including Amazonia, Yucatan, West-Central Africa, Sri Lanka, and New Caledonia, with a negligible island effect compared with plants and animals. We also found that fungi are predominantly vulnerable to drought, heat and land-cover change, particularly in dry tropical regions with high human population density. Fungal conservation areas of highest priority include herbaceous wetlands, tropical forests, and woodlands. We stress that more attention should be focused on the conservation of fungi, especially root symbiotic arbuscular mycorrhizal and ectomycorrhizal fungi in tropical regions as well as unicellular early-diverging groups and macrofungi in general. Given the low overlap between the endemicity of fungi and macroorganisms, but high conservation needs in both groups, detailed analyses on distribution and conservation requirements are warranted for other microorganisms and soil organisms.