Unforeseen plant phenotypic diversity in a dry and grazed world.

Earth harbours an extraordinary plant phenotypic diversity1 that is at risk from ongoing global changes2,3. However, it remains unknown how increasing aridity and livestock grazing pressure-two major drivers of global change4-6-shape the trait covariation that underlies plant phenotypic diversity1,7. Here we assessed how covariation among 20 chemical and morphological traits responds to aridity and grazing pressure within global drylands. Our analysis involved 133,769 trait measurements spanning 1,347 observations of 301 perennial plant species surveyed across 326 plots from 6 continents. Crossing an aridity threshold of approximately 0.7 (close to the transition between semi-arid and arid zones) led to an unexpected 88% increase in trait diversity. This threshold appeared in the presence of grazers, and moved toward lower aridity levels with increasing grazing pressure. Moreover, 57% of observed trait diversity occurred only in the most arid and grazed drylands, highlighting the phenotypic uniqueness of these extreme environments. Our work indicates that drylands act as a global reservoir of plant phenotypic diversity and challenge the pervasive view that harsh environmental conditions reduce plant trait diversity8-10. They also highlight that many alternative strategies may enable plants to cope with increases in environmental stress induced by climate change and land-use intensification.

Global hotspots for soil nature conservation.

Soils are the foundation of all terrestrial ecosystems1. However, unlike for plants and animals, a global assessment of hotspots for soil nature conservation is still lacking2. This hampers our ability to establish nature conservation priorities for the multiple dimensions that support the soil system: from soil biodiversity to ecosystem services. Here, to identify global hotspots for soil nature conservation, we performed a global field survey that includes observations of biodiversity (archaea, bacteria, fungi, protists and invertebrates) and functions (critical for six ecosystem services) in 615 composite samples of topsoil from a standardized survey in all continents. We found that each of the different ecological dimensions of soils-that is, species richness (alpha diversity, measured as amplicon sequence variants), community dissimilarity and ecosystem services-peaked in contrasting regions of the planet, and were associated with different environmental factors. Temperate ecosystems showed the highest species richness, whereas community dissimilarity peaked in the tropics, and colder high-latitudinal ecosystems were identified as hotspots of ecosystem services. These findings highlight the complexities that are involved in simultaneously protecting multiple ecological dimensions of soil. We further show that most of these hotspots are not adequately covered by protected areas (more than 70%), and are vulnerable in the context of several scenarios of global change. Our global estimation of priorities for soil nature conservation highlights the importance of accounting for the multidimensionality of soil biodiversity and ecosystem services to conserve soils for future generations.

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.

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.

Prevalence and drivers of abrupt vegetation shifts in global drylands.

The constant provision of plant productivity is integral to supporting the liability of ecosystems and human wellbeing in global drylands. Drylands are paradigmatic examples of systems prone to experiencing abrupt changes in their functioning. Indeed, space-for-time substitution approaches suggest that abrupt changes in plant productivity are widespread, but this evidence is less clear using observational time series or experimental data at a large scale. Studying the prevalence and, most importantly, the unknown drivers of abrupt (rather than gradual) dynamical patterns in drylands may help to unveil hotspots of current and future dynamical instabilities in drylands. Using a 20-y global satellite-derived temporal assessment of dryland Normalized Difference Vegetation Index (NDVI), we show that 50% of all dryland ecosystems exhibiting gains or losses of NDVI are characterized by abrupt positive/negative temporal dynamics. We further show that abrupt changes are more common among negative than positive NDVI trends and can be found in global regions suffering recent droughts, particularly around critical aridity thresholds. Positive abrupt dynamics are found most in ecosystems with low seasonal variability or high aridity. Our work unveils the high importance of climate variability on triggering abrupt shifts in vegetation and it provides missing evidence of increasing abruptness in systems intensively managed by humans, with low soil organic carbon contents, or around specific aridity thresholds. These results highlight that abrupt changes in dryland dynamics are very common, especially for productivity losses, pinpoint global hotspots of dryland vulnerability, and identify drivers that could be targeted for effective dryland management.

Aridity-dependent shifts in biodiversity-stability relationships but not in underlying mechanisms.

Climate change will affect the way biodiversity influences the stability of plant communities. Although biodiversity, associated species asynchrony, and species stability could enhance community stability, the understanding of potential nonlinear shifts in the biodiversity-stability relationship across a wide range of aridity (measured as the aridity index, the precipitation/potential evapotranspiration ratio) gradients and the underlying mechanisms remain limited. Using an 8-year dataset from 687 sites in Mongolia, which included 5496 records of vegetation and productivity, we found that the temporal stability of plant communities decreased more rapidly in more arid areas than in less arid areas. The result suggests that future aridification across terrestrial ecosystems may adversely affect community stability. Additionally, we identified nonlinear shifts in the effects of species richness and species synchrony on temporal community stability along the aridity gradient. Species synchrony was a primary driver of community stability, which was consistently negatively affected by species richness while being positively affected by the synchrony between C3 and C4 species across the aridity gradient. These results highlight the crucial role of C4 species in stabilizing communities through differential responses to interannual climate variations between C3 and C4 species. Notably, species richness and the synchrony between C3 and C4 species independently regulated species synchrony, ultimately affecting community stability. We propose that maintaining plant communities with a high diversity of C3 and C4 species will be key to enhancing community stability across Mongolian grasslands. Moreover, species synchrony, species stability, species richness and the synchrony between C3 and C4 species across the aridity gradient consistently mediated the impacts of aridity on community stability. Hence, strategies aimed at promoting the maintenance of biological diversity and composition will help ecosystems adapt to climate change or mitigate its adverse effects on ecosystem stability.

Unearthing the soil-borne microbiome of land plants.

Plant-soil biodiversity interactions are fundamental for the functioning of terrestrial ecosystems. Yet, the existence of a set of globally distributed topsoil microbial and small invertebrate organisms consistently associated with land plants (i.e., their consistent soil-borne microbiome), together with the environmental preferences and functional capabilities of these organisms, remains unknown. We conducted a standardized field survey under 150 species of land plants, including 58 species of bryophytes and 92 of vascular plants, across 124 locations from all continents. We found that, despite the immense biodiversity of soil organisms, the land plants evaluated only shared a small fraction (less than 1%) of all microbial and invertebrate taxa that were present across contrasting climatic and soil conditions and vegetation types. These consistent taxa were dominated by generalist decomposers and phagotrophs and their presence was positively correlated with the abundance of functional genes linked to mineralization. Finally, we showed that crossing environmental thresholds in aridity (aridity index of 0.65, i.e., the transition from mesic to dry ecosystems), soil pH (5.5; i.e., the transition from acidic to strongly acidic soils), and carbon (less than 2%, the lower limit of fertile soils) can result in drastic disruptions in the associations between land plants and soil organisms, with potential implications for the delivery of soil ecosystem processes under ongoing global environmental change.

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.

Temperature thresholds drive the global distribution of soil fungal decomposers.

Unraveling the biogeographic pattern of soil fungal decomposers along temperature gradients-in smooth linearity or an abrupt jump-can help us connect the global carbon cycle to global warming. Through a standardized global field survey, we identify the existence of temperature thresholds that control the global distribution of soil fungal decomposers, leading to abrupt reductions in their proportion (i.e., the relative abundance in the fungal community) immediately after crossing particular air and soil temperature thresholds. For example, small increases over the mean annual temperature threshold of ~9°C result in abrupt reductions in their proportion, paralleling a similar temperature threshold for soil carbon content. We further find that the proportion of soil fungal decomposers is more sensitive to temperature increases under arid conditions. Given the positive correlation between the global distributions of fungal decomposers and soil heterotrophic respiration, the reported temperature-driven abrupt reductions in fungal decomposers could further suppress their driven soil decomposition processes and reduce carbon fluxes from soils to the atmosphere with implications for climate change feedback. This work not only advances the current knowledge on the global distribution of soil fungal decomposers, but also highlights that small changes in temperature around certain thresholds can lead to potential unexpected consequences in global carbon cycling under projected climate change.

Phylogenetic, functional, and taxonomic richness have both positive and negative effects on ecosystem multifunctionality.

Biodiversity encompasses multiple attributes such as the richness and abundance of species (taxonomic diversity), the presence of different evolutionary lineages (phylogenetic diversity), and the variety of growth forms and resource use strategies (functional diversity). These biodiversity attributes do not necessarily relate to each other and may have contrasting effects on ecosystem functioning. However, how they simultaneously influence the provision of multiple ecosystem functions related to carbon, nitrogen, and phosphorus cycling (multifunctionality) remains unknown. We evaluated the effects of the taxonomic, phylogenetic, and functional attributes of dominant (mass ratio effects) and subordinate (richness effect) plant species on the multifunctionality of 123 drylands from six continents. Our results highlight the importance of the phylogenetic and functional attributes of subordinate species as key drivers of multifunctionality. In addition to a higher taxonomic richness, we found that simultaneously increasing the richness of early diverging lineages and the functional redundancy between species increased multifunctionality. In contrast, the richness of most recent evolutionary lineages and the functional and phylogenetic attributes of dominant plant species (mass ratio effects) were weakly correlated with multifunctionality. However, they were important drivers of individual nutrient cycles. By identifying which biodiversity attributes contribute the most to multifunctionality, our results can guide restoration efforts aiming to maximize either multifunctionality or particular nutrient cycles, a critical step to combat dryland desertification worldwide.

Biogeography of global drylands.

Despite their extent and socio-ecological importance, a comprehensive biogeographical synthesis of drylands is lacking. Here we synthesize the biogeography of key organisms (vascular and nonvascular vegetation and soil microorganisms), attributes (functional traits, spatial patterns, plant-plant and plant-soil interactions) and processes (productivity and land cover) across global drylands. These areas have a long evolutionary history, are centers of diversification for many plant lineages and include important plant diversity hotspots. This diversity captures a strikingly high portion of the variation in leaf functional diversity observed globally. Part of this functional diversity is associated with the large variation in response and effect traits in the shrubs encroaching dryland grasslands. Aridity and its interplay with the traits of interacting plant species largely shape biogeographical patterns in plant-plant and plant-soil interactions, and in plant spatial patterns. Aridity also drives the composition of biocrust communities and vegetation productivity, which shows large geographical variation. We finish our review by discussing major research gaps, which include: studying regular vegetation spatial patterns; establishing large-scale plant and biocrust field surveys assessing individual-level trait measurements; knowing whether the impacts of plant-plant and plant-soil interactions on biodiversity are predictable; and assessing how elevated CO2 modulates future aridity conditions and plant productivity.

Decoupling of soil nutrient cycles as a function of aridity in global drylands.

The biogeochemical cycles of carbon (C), nitrogen (N) and phosphorus (P) are interlinked by primary production, respiration and decomposition in terrestrial ecosystems. It has been suggested that the C, N and P cycles could become uncoupled under rapid climate change because of the different degrees of control exerted on the supply of these elements by biological and geochemical processes. Climatic controls on biogeochemical cycles are particularly relevant in arid, semi-arid and dry sub-humid ecosystems (drylands) because their biological activity is mainly driven by water availability. The increase in aridity predicted for the twenty-first century in many drylands worldwide may therefore threaten the balance between these cycles, differentially affecting the availability of essential nutrients. Here we evaluate how aridity affects the balance between C, N and P in soils collected from 224 dryland sites from all continents except Antarctica. We find a negative effect of aridity on the concentration of soil organic C and total N, but a positive effect on the concentration of inorganic P. Aridity is negatively related to plant cover, which may favour the dominance of physical processes such as rock weathering, a major source of P to ecosystems, over biological processes that provide more C and N, such as litter decomposition. Our findings suggest that any predicted increase in aridity with climate change will probably reduce the concentrations of N and C in global drylands, but increase that of P. These changes would uncouple the C, N and P cycles in drylands and could negatively affect the provision of key services provided by these ecosystems.

Structure and functioning of dryland ecosystems in a changing world.

Understanding how drylands respond to ongoing environmental change is extremely important for global sustainability. Here we review how biotic attributes, climate, grazing pressure, land cover change and nitrogen deposition affect the functioning of drylands at multiple spatial scales. Our synthesis highlights the importance of biotic attributes (e.g. species richness) in maintaining fundamental ecosystem processes such as primary productivity, illustrate how N deposition and grazing pressure are impacting ecosystem functioning in drylands worldwide, and highlight the importance of the traits of woody species as drivers of their expansion in former grasslands. We also emphasize the role of attributes such as species richness and abundance in controlling the responses of ecosystem functioning to climate change. This knowledge is essential to guide conservation and restoration efforts in drylands, as biotic attributes can be actively managed at the local scale to increase ecosystem resilience to global change.

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.

Can we infer plant facilitation from remote sensing? a test across global drylands.

Facilitation is a major force shaping the structure and diversity of plant communities in terrestrial ecosystems. Detecting positive plant-plant interactions relies on the combination of field experimentation and the demonstration of spatial association between neighboring plants. This has often restricted the study of facilitation to particular sites, limiting the development of systematic assessments of facilitation over regional and global scales. Here we explore whether the frequency of plant spatial associations detected from high-resolution remotely sensed images can be used to infer plant facilitation at the community level in drylands around the globe. We correlated the information from remotely sensed images freely available through Google Earth with detailed field assessments, and used a simple individual-based model to generate patch-size distributions using different assumptions about the type and strength of plant-plant interactions. Most of the patterns found from the remotely sensed images were more right skewed than the patterns from the null model simulating a random distribution. This suggests that the plants in the studied drylands show stronger spatial clustering than expected by chance. We found that positive plant co-occurrence, as measured in the field, was significantly related to the skewness of vegetation patch-size distribution measured using Google Earth images. Our findings suggest that the relative frequency of facilitation may be inferred from spatial pattern signals measured from remotely sensed images, since facilitation often determines positive co-occurrence among neighboring plants. They pave the road for a systematic global assessment of the role of facilitation in terrestrial ecosystems.

Positive feedbacks and alternative stable states in forest leaf types.

The emergence of alternative stable states in forest systems has significant implications for the functioning and structure of the terrestrial biosphere, yet empirical evidence remains scarce. Here, we combine global forest biodiversity observations and simulations to test for alternative stable states in the presence of evergreen and deciduous forest types. We reveal a bimodal distribution of forest leaf types across temperate regions of the Northern Hemisphere that cannot be explained by the environment alone, suggesting signatures of alternative forest states. Moreover, we empirically demonstrate the existence of positive feedbacks in tree growth, recruitment and mortality, with trees having 4-43% higher growth rates, 14-17% higher survival rates and 4-7 times higher recruitment rates when they are surrounded by trees of their own leaf type. Simulations show that the observed positive feedbacks are necessary and sufficient to generate alternative forest states, which also lead to dependency on history (hysteresis) during ecosystem transition from evergreen to deciduous forests and vice versa. We identify hotspots of bistable forest types in evergreen-deciduous ecotones, which are likely driven by soil-related positive feedbacks. These findings are integral to predicting the distribution of forest biomes, and aid to our understanding of biodiversity, carbon turnover, and terrestrial climate feedbacks.

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.

Changes in biocrust cover drive carbon cycle responses to climate change in drylands.

Dryland ecosystems account for ca. 27% of global soil organic carbon (C) reserves, yet it is largely unknown how climate change will impact C cycling and storage in these areas. In drylands, soil C concentrates at the surface, making it particularly sensitive to the activity of organisms inhabiting the soil uppermost levels, such as communities dominated by lichens, mosses, bacteria and fungi (biocrusts). We conducted a full factorial warming and rainfall exclusion experiment at two semiarid sites in Spain to show how an average increase of air temperature of 2-3 °C promoted a drastic reduction in biocrust cover (ca. 44% in 4 years). Warming significantly increased soil CO2 efflux, and reduced soil net CO2 uptake, in biocrust-dominated microsites. Losses of biocrust cover with warming through time were paralleled by increases in recalcitrant C sources, such as aromatic compounds, and in the abundance of fungi relative to bacteria. The dramatic reduction in biocrust cover with warming will lessen the capacity of drylands to sequester atmospheric CO2 . This decrease may act synergistically with other warming-induced effects, such as the increase in soil CO2 efflux and the changes in microbial communities to alter C cycling in drylands, and to reduce soil C stocks in the mid to long term.

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.

Widespread synchronous decline of Mediterranean-type forest driven by accelerated aridity.

Large-scale, abrupt ecosystem change in direct response to climate extremes is a critical but poorly documented phenomenon1. Yet, recent increases in climate-induced tree mortality raise concern that some forest ecosystems are on the brink of collapse across wide environmental gradients2,3. Here we assessed climatic and productivity trends across the world's five Mediterranean forest ecosystems from 2000 to 2021 and detected a large-scale, abrupt forest browning and productivity decline in Chile (>90% of the forest in <100 days), responding to a sustained, acute drought. The extreme dry and warm conditions in Chile, unprecedented in the recent history of all Mediterranean-type ecosystems, are akin to those projected to arise in the second half of the century4. Long-term recovery of this forest is uncertain given an ongoing decline in regional water balance. This dramatic plummet of forest productivity may be a spyglass to the future for other Mediterranean ecosystems.