Hotspots of biogeochemical activity linked to aridity and plant traits across global drylands.

Perennial plants create productive and biodiverse hotspots, known as fertile islands, beneath their canopies. These hotspots largely determine the structure and functioning of drylands worldwide. Despite their ubiquity, the factors controlling fertile islands under conditions of contrasting grazing by livestock, the most prevalent land use in drylands, remain virtually unknown. Here we evaluated the relative importance of grazing pressure and herbivore type, climate and plant functional traits on 24 soil physical and chemical attributes that represent proxies of key ecosystem services related to decomposition, soil fertility, and soil and water conservation. To do this, we conducted a standardized global survey of 288 plots at 88 sites in 25 countries worldwide. We show that aridity and plant traits are the major factors associated with the magnitude of plant effects on fertile islands in grazed drylands worldwide. Grazing pressure had little influence on the capacity of plants to support fertile islands. Taller and wider shrubs and grasses supported stronger island effects. Stable and functional soils tended to be linked to species-rich sites with taller plants. Together, our findings dispel the notion that grazing pressure or herbivore type are linked to the formation or intensification of fertile islands in drylands. Rather, our study suggests that changes in aridity, and processes that alter island identity and therefore plant traits, will have marked effects on how perennial plants support and maintain the functioning of drylands in a more arid and grazed world.

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.

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.

Fourteen years of continuous soil moisture records from plant and biocrust-dominated microsites.

Drylands cover ~41% of the terrestrial surface. In these water-limited ecosystems, soil moisture contributes to multiple hydrological processes and is a crucial determinant of the activity and performance of above- and belowground organisms and of the ecosystem processes that rely on them. Thus, an accurate characterisation of the temporal dynamics of soil moisture is critical to improve our understanding of how dryland ecosystems function and are responding to ongoing climate change. Furthermore, it may help improve climatic forecasts and drought monitoring. Here we present the MOISCRUST dataset, a long-term (2006-2020) soil moisture dataset at a sub-daily resolution from five different microsites (vascular plants and biocrusts) in a Mediterranean semiarid dryland located in Central Spain. MOISCRUST is a unique dataset for improving our understanding on how both vascular plants and biocrusts determine soil water dynamics in drylands, and thus to better assess their hydrological impacts and responses to ongoing climate change.

Effects of vegetation on soil cyanobacterial communities through time and space.

Photoautotrophic soil cyanobacteria play essential ecological roles and are known to exhibit large changes in their diversity and abundance throughout early succession. However, much less is known about how and why soil cyanobacterial communities change as soil develops over centuries and millennia, and the effects that vegetation have on such communities. We combined an extensive field survey, including 16 global soil chronosequences across contrasting ecosystems (from deserts to tropical forests), with molecular analyses to investigate how the diversity and abundance of photosynthetic and nonphotosynthetic soil cyanobacteria are affected by vegetation change during soil development, over time periods from hundreds to thousands of years. We show that, in most chronosequences, the abundance, species richness and community composition of soil cyanobacteria are relatively stable as soil develops (from centuries to millennia). Regardless of soil age, forest chronosequences were consistently dominated by nonphotosynthetic cyanobacteria (Vampirovibrionia), while grasslands and shrublands were dominated by photosynthetic cyanobacteria. Chronosequences undergoing drastic vegetation shifts (e.g. transitions from grasslands to forests) experienced significant changes in the composition of soil cyanobacterial communities. Our results advance our understanding of the ecology of cyanobacterial classes, and of the understudied nonphotosynthetic cyanobacteria in particular, and highlight the key role of vegetation as a major driver of their temporal dynamics as soil develops.

Functional rarity and evenness are key facets of biodiversity to boost multifunctionality.

The functional traits of organisms within multispecies assemblages regulate biodiversity effects on ecosystem functioning. Yet how traits should assemble to boost multiple ecosystem functions simultaneously (multifunctionality) remains poorly explored. In a multibiome litter experiment covering most of the global variation in leaf trait spectra, we showed that three dimensions of functional diversity (dispersion, rarity, and evenness) explained up to 66% of variations in multifunctionality, although the dominant species and their traits remained an important predictor. While high dispersion impeded multifunctionality, increasing the evenness among functionally dissimilar species was a key dimension to promote higher multifunctionality and to reduce the abundance of plant pathogens. Because too-dissimilar species could have negative effects on ecosystems, our results highlight the need for not only diverse but also functionally even assemblages to promote multifunctionality. The effect of functionally rare species strongly shifted from positive to negative depending on their trait differences with the dominant species. Simultaneously managing the dispersion, evenness, and rarity in multispecies assemblages could be used to design assemblages aimed at maximizing multifunctionality independently of the biome, the identity of dominant species, or the range of trait values considered. Functional evenness and rarity offer promise to improve the management of terrestrial ecosystems and to limit plant disease risks.

Species-specific effects of biocrust-forming lichens on soil properties under simulated climate change are driven by functional traits.

Biocrusts are key drivers of ecosystem functioning in drylands, yet our understanding of how climate change will affect the chemistry of biocrust-forming species and their impacts on carbon (C) and nitrogen (N) cycling is still very limited. Using a manipulative experiment conducted with common biocrust-forming lichens with distinct morphology and chemistry (Buellia zoharyi, Diploschistes diacapsis, Psora decipiens and Squamarina lentigera), we evaluated changes in lichen total and isotopic C and N and several soil C and N variables after 50 months of simulated warming and rainfall reduction. Climate change treatments reduced δ13 C and the C : N ratio in B. zoharyi, and increased δ15 N in S. lentigera. Lichens had species-specific effects on soil dissolved organic N (DON), NH4+ , ß-glucosidase and acid phosphatase activity regardless of climate change treatments, while these treatments changed how lichens affected several soil properties regardless of biocrust species. Changes in thallus δ13 C, N and C : N drove species-specific effects on dissolved organic nitrogen (DON), NH4+ , ß-glucosidase and acid phosphatase activity. Our findings indicate that warmer and drier conditions will alter the chemistry of biocrust-forming lichens, affecting soil nutrient cycling, and emphasize their key role as modulators of climate change impacts in dryland soils.

Contrasting mechanisms underlie short- and longer-term soil respiration responses to experimental warming in a dryland ecosystem.

Soil carbon losses to the atmosphere through soil respiration are expected to rise with ongoing temperature increases, but available evidence from mesic biomes suggests that such response disappears after a few years of experimental warming. However, there is lack of empirical basis for these temporal dynamics in soil respiration responses, and for the mechanisms underlying them, in drylands, which collectively form the largest biome on Earth and store 32% of the global soil organic carbon pool. We coupled data from a 10 year warming experiment in a biocrust-dominated dryland ecosystem with laboratory incubations to confront 0-2 years (short-term hereafter) versus 8-10 years (longer-term hereafter) soil respiration responses to warming. Our results showed that increased soil respiration rates with short-term warming observed in areas with high biocrust cover returned to control levels in the longer-term. Warming-induced increases in soil temperature were the main drivers of the short-term soil respiration responses, whereas longer-term soil respiration responses to warming were primarily driven by thermal acclimation and warming-induced reductions in biocrust cover. Our results highlight the importance of evaluating short- and longer-term soil respiration responses to warming as a mean to reduce the uncertainty in predicting the soil carbon-climate feedback in drylands.

Biocrusts buffer against the accumulation of soil metallic nutrients induced by warming and rainfall reduction.

The availability of metallic nutrients in dryland soils, many of which are essential for the metabolism of soil organisms and vascular plants, may be altered due to climate change-driven increases in aridity. Biocrusts, soil surface communities dominated by lichens, bryophytes and cyanobacteria, are ecosystem engineers known to exert critical functions in dryland ecosystems. However, their role in regulating metallic nutrient availability under climate change is uncertain. Here, we evaluated whether well-developed biocrusts modulate metallic nutrient availability in response to 7 years of experimental warming and rainfall reduction in a Mediterranean dryland located in southeastern Spain. We found increases in the availability of K, Mg, Zn and Na under warming and rainfall exclusion. However, the presence of a well-developed biocrust cover buffered these effects, most likely because its constituents can uptake significant quantities of available metallic nutrients. Our findings suggest that biocrusts, a biotic community prevalent in drylands, exert an important role in preserving and protecting metallic nutrients in dryland soils from leaching and erosion. Therefore, we highlight the need to protect them to mitigate undesired effects of soil degradation driven by climate change in this globally expanding biome.

Cascading effects from plants to soil microorganisms explain how plant species richness and simulated climate change affect soil multifunctionality.

Despite their importance, how plant communities and soil microorganisms interact to determine the capacity of ecosystems to provide multiple functions simultaneously (multifunctionality) under climate change is poorly known. We conducted a common garden experiment using grassland species to evaluate how plant functional structure and soil microbial (bacteria and protists) diversity and abundance regulate soil multifunctionality responses to joint changes in plant species richness (one, three and six species) and simulated climate change (3°C warming and 35% rainfall reduction). The effects of species richness and climate on soil multifunctionality were indirectly driven via changes in plant functional structure and their relationships with the abundance and diversity of soil bacteria and protists. More specifically, warming selected for the larger and most productive plant species, increasing the average size within communities and leading to reductions in functional plant diversity. These changes increased the total abundance of bacteria that, in turn, increased that of protists, ultimately promoting soil multifunctionality. Our work suggests that cascading effects between plant functional traits and the abundance of multitrophic soil organisms largely regulate the response of soil multifunctionality to simulated climate change, and ultimately provides novel experimental insights into the mechanisms underlying the effects of biodiversity and climate change on ecosystem functioning.

Pathways regulating decreased soil respiration with warming in a biocrust-dominated dryland.

A positive soil carbon (C)-climate feedback is embedded into the climatic models of the IPCC. However, recent global syntheses indicate that the temperature sensitivity of soil respiration (RS ) in drylands, the largest biome on Earth, is actually lower in warmed than in control plots. Consequently, soil C losses with future warming are expected to be low compared with other biomes. Nevertheless, the empirical basis for these global extrapolations is still poor in drylands, due to the low number of field experiments testing the pathways behind the long-term responses of soil respiration (RS ) to warming. Importantly, global drylands are covered with biocrusts (communities formed by bryophytes, lichens, cyanobacteria, fungi, and bacteria), and thus, RS responses to warming may be driven by both autotrophic and heterotrophic pathways. Here, we evaluated the effects of 8-year experimental warming on RS , and the different pathways involved, in a biocrust-dominated dryland in southern Spain. We also assessed the overall impacts on soil organic C (SOC) accumulation over time. Across the years and biocrust cover levels, warming reduced RS by 0.30 µmol CO2  m-2  s-1 (95% CI = -0.24 to 0.84), although the negative warming effects were only significant after 3 years of elevated temperatures in areas with low initial biocrust cover. We found support for different pathways regulating the warming-induced reduction in RS at areas with low (microbial thermal acclimation via reduced soil mass-specific respiration and ß-glucosidase enzymatic activity) vs. high (microbial thermal acclimation jointly with a reduction in autotrophic respiration from decreased lichen cover) initial biocrust cover. Our 8-year experimental study shows a reduction in soil respiration with warming and highlights that biocrusts should be explicitly included in modeling efforts aimed to quantify the soil C-climate feedback in drylands.

Soil microbial communities drive the resistance of ecosystem multifunctionality to global change in drylands across the globe.

The relationship between soil microbial communities and the resistance of multiple ecosystem functions linked to C, N and P cycling (multifunctionality resistance) to global change has never been assessed globally in natural ecosystems. We collected soils from 59 dryland ecosystems worldwide to investigate the importance of microbial communities as predictor of multifunctionality resistance to climate change and nitrogen fertilisation. Multifunctionality had a lower resistance to wetting-drying cycles than to warming or N deposition. Multifunctionality resistance was regulated by changes in microbial composition (relative abundance of phylotypes) but not by richness, total abundance of fungi and bacteria or the fungal: bacterial ratio. Our results suggest that positive effects of particular microbial taxa on multifunctionality resistance could potentially be controlled by altering soil pH. Together, our work demonstrates strong links between microbial community composition and multifunctionality resistance in dryland soils from six continents, and provides insights into the importance of microbial community composition for buffering effects of global change in drylands worldwide.

Biocrust-forming mosses mitigate the negative impacts of increasing aridity on ecosystem multifunctionality in drylands.

The increase in aridity predicted with climate change will have a negative impact on the multiple functions and services (multifunctionality) provided by dryland ecosystems worldwide. In these ecosystems, soil communities dominated by mosses, lichens and cyanobacteria (biocrusts) play a key role in supporting multifunctionality. However, whether biocrusts can buffer the negative impacts of aridity on important biogeochemical processes controlling carbon (C), nitrogen (N), and phosphorus (P) pools and fluxes remains largely unknown. Here, we conducted an empirical study, using samples from three continents (North America, Europe and Australia), to evaluate how the increase in aridity predicted by climate change will alter the capacity of biocrust-forming mosses to modulate multiple ecosystem processes related to C, N and P cycles. Compared with soil surfaces lacking biocrusts, biocrust-forming mosses enhanced multiple functions related to C, N and P cycling and storage in semiarid and arid, but not in humid and dry-subhumid, environments. Most importantly, we found that the relative positive effects of biocrust-forming mosses on multifunctionality compared with bare soil increased with increasing aridity. These results were mediated by plant cover and the positive effects exerted by biocrust-forming mosses on the abundance of soil bacteria and fungi. Our findings provide strong evidence that the maintenance of biocrusts is crucial to buffer negative effects of climate change on multifunctionality in global drylands.

Increasing aridity reduces soil microbial diversity and abundance in global drylands.

Soil bacteria and fungi play key roles in the functioning of terrestrial ecosystems, yet our understanding of their responses to climate change lags significantly behind that of other organisms. This gap in our understanding is particularly true for drylands, which occupy ∼41% of Earth´s surface, because no global, systematic assessments of the joint diversity of soil bacteria and fungi have been conducted in these environments to date. Here we present results from a study conducted across 80 dryland sites from all continents, except Antarctica, to assess how changes in aridity affect the composition, abundance, and diversity of soil bacteria and fungi. The diversity and abundance of soil bacteria and fungi was reduced as aridity increased. These results were largely driven by the negative impacts of aridity on soil organic carbon content, which positively affected the abundance and diversity of both bacteria and fungi. Aridity promoted shifts in the composition of soil bacteria, with increases in the relative abundance of Chloroflexi and α-Proteobacteria and decreases in Acidobacteria and Verrucomicrobia. Contrary to what has been reported by previous continental and global-scale studies, soil pH was not a major driver of bacterial diversity, and fungal communities were dominated by Ascomycota. Our results fill a critical gap in our understanding of soil microbial communities in terrestrial ecosystems. They suggest that changes in aridity, such as those predicted by climate-change models, may reduce microbial abundance and diversity, a response that will likely impact the provision of key ecosystem services by global drylands.

Warming reduces the cover and diversity of biocrust-forming mosses and lichens, and increases the physiological stress of soil microbial communities in a semi-arid Pinus halepensis plantation.

Soil communities dominated by lichens and mosses (biocrusts) play key roles in maintaining ecosystem structure and functioning in drylands worldwide. However, few studies have explicitly evaluated how climate change-induced impacts on biocrusts affect associated soil microbial communities. We report results from a field experiment conducted in a semiarid Pinus halepensis plantation, where we setup an experiment with two factors: cover of biocrusts (low [<15%] versus high [>50%]), and warming (control versus a ∼2°C temperature increase). Warming reduced the richness and cover (∼45%) of high biocrust cover areas 53 months after the onset of the experiment. This treatment did not change the ratios between the major microbial groups, as measured by phospholipid fatty acid analysis. Warming increased the physiological stress of the Gram negative bacterial community, as indicated by the cy17:0/16:1ω7 ratio. This response was modulated by the initial biocrust cover, as the increase in this ratio with warming was higher in areas with low cover. Our findings suggest that biocrusts can slow down the negative effects of warming on the physiological status of the Gram negative bacterial community. However, as warming will likely reduce the cover and diversity of biocrusts, these positive effects will be reduced under climate change.

Intransitive competition is widespread in plant communities and maintains their species richness.

Intransitive competition networks, those in which there is no single best competitor, may ensure species coexistence. However, their frequency and importance in maintaining diversity in real-world ecosystems remain unclear. We used two large data sets from drylands and agricultural grasslands to assess: (1) the generality of intransitive competition, (2) intransitivity-richness relationships and (3) effects of two major drivers of biodiversity loss (aridity and land-use intensification) on intransitivity and species richness. Intransitive competition occurred in > 65% of sites and was associated with higher species richness. Intransitivity increased with aridity, partly buffering its negative effects on diversity, but was decreased by intensive land use, enhancing its negative effects on diversity. These contrasting responses likely arise because intransitivity is promoted by temporal heterogeneity, which is enhanced by aridity but may decline with land-use intensity. We show that intransitivity is widespread in nature and increases diversity, but it can be lost with environmental homogenisation.

Separating natural from anthropogenic causes of impairment in Zebra mussel (Dreissena polymorpha) populations living across a pollution gradient.

The relationship between the reproductive stage, the total lipid content and eight broadly used biochemical stress responses were used to assess seasonal and pollutant effects across eleven different zebra mussel (Dreissena polymorpha) populations from the Ebro and Mijares river basin, Spain. Biochemical markers included superoxide dismutase (SOD), catalase (CAT), glutathione (GSH), glutathione S transferase (GST), multixenobiotic transporter activity (MXR), lactate dehydrogenase (LDH), lipid peroxidation (LPO) and single strand DNA breaks. Principal component analyses of zebra mussel responses across an annual cycle, showed a marked gonad stage component in total lipid content and biochemical responses. The same response pattern was observed across the populations sampled along a broad geographical and pollution gradient. Population differences on the gonad developmental stage were highly correlated with most of the measured responses and unrelated with the pollution gradient. Conversely, bioaccumulation of organic and inorganic contaminant residues was more related to pollution sources than with the reproductive cycle. These results indicate that the reproductive cycle is the major factor affecting the temporal and spatial variation of the studied markers in D. polymorpha.