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.

Plant-soil synchrony in nutrient cycles: Learning from ecosystems to design sustainable agrosystems.

Redesigning agrosystems to include more ecological regulations can help feed a growing human population, preserve soils for future productivity, limit dependency on synthetic fertilizers, and reduce agriculture contribution to global changes such as eutrophication and warming. However, guidelines for redesigning cropping systems from natural systems to make them more sustainable remain limited. Synthetizing the knowledge on biogeochemical cycles in natural ecosystems, we outline four ecological systems that synchronize the supply of soluble nutrients by soil biota with the fluctuating nutrient demand of plants. This synchrony limits deficiencies and excesses of soluble nutrients, which usually penalize both production and regulating services of agrosystems such as nutrient retention and soil carbon storage. In the ecological systems outlined, synchrony emerges from plant-soil and plant-plant interactions, eco-physiological processes, soil physicochemical processes, and the dynamics of various nutrient reservoirs, including soil organic matter, soil minerals, atmosphere, and a common market. We discuss the relative importance of these ecological systems in regulating nutrient cycles depending on the pedoclimatic context and on the functional diversity of plants and microbes. We offer ideas about how these systems could be stimulated within agrosystems to improve their sustainability. A review of the latest advances in agronomy shows that some of the practices suggested to promote synchrony (e.g., reduced tillage, rotation with perennial plant cover, crop diversification) have already been tested and shown to be effective in reducing nutrient losses, fertilizer use, and N2 O emissions and/or improving biomass production and soil carbon storage. Our framework also highlights new management strategies and defines the conditions for the success of these nature-based practices allowing for site-specific modifications. This new synthetized knowledge should help practitioners to improve the long-term productivity of agrosystems while reducing the negative impact of agriculture on the environment and the climate.

Biodiversity and pollination benefits trade off against profit in an intensive farming system.

Agricultural expansion and intensification have boosted global food production but have come at the cost of environmental degradation and biodiversity loss. Biodiversity-friendly farming that boosts ecosystem services, such as pollination and natural pest control, is widely being advocated to maintain and improve agricultural productivity while safeguarding biodiversity. A vast body of evidence showing the agronomic benefits of enhanced ecosystem service delivery represent important incentives to adopt practices enhancing biodiversity. However, the costs of biodiversity-friendly management are rarely taken into account and may represent a major barrier impeding uptake by farmers. Whether and how biodiversity conservation, ecosystem service delivery, and farm profit can go hand in hand is unknown. Here, we quantify the ecological, agronomic, and net economic benefits of biodiversity-friendly farming in an intensive grassland-sunflower system in Southwest France. We found that reducing land-use intensity on agricultural grasslands drastically enhances flower availability and wild bee diversity, including rare species. Biodiversity-friendly management on grasslands furthermore resulted in an up to 17% higher revenue on neighboring sunflower fields through positive effects on pollination service delivery. However, the opportunity costs of reduced grassland forage yields consistently exceeded the economic benefits of enhanced sunflower pollination. Our results highlight that profitability is often a key constraint hampering adoption of biodiversity-based farming and uptake critically depends on society's willingness to pay for associated delivery of public goods such as biodiversity.

Species richness drives selection of individuals within wetlands based on traits related to acquisition and utilization of light.

Selection within natural communities has mainly been studied along large abiotic gradients, while the selection of individuals within populations should occur locally in response to biotic filters. To better leverage the role of the latter, we considered the hierarchal nature of environmental selection for the multiple dimensions of the trait space across biological levels, that is, from the species to the community and the ecosystem levels. We replicated a natural species richness gradient where communities included from two to 16 species within four wetlands (bog, fen, meadow, and marsh) contrasting in plant productivity. We sampled functional traits from individuals in each community and used hierarchical distributional modeling in order to analyze the independent variation of the mean and dispersion of functional trait space at ecosystem, community, and species levels. The plant productivity gradient observed between wetlands led to species turnover and selection of traits related to leaf nutrient conservation/acquisition strategy. Within wetlands, plant species richness drove trait variation across both communities and species. Among communities, variation of species richness correlated with the selection of individuals according to their use of vertical space and leaf adaptations to light conditions. Within species, intraspecific light-related trait variation in response to species richness was associated with stable population density for some species, while others reached low population density in more diverse communities. Within ecosystems, variation in biotic conditions selects individuals along functional dimensions that are independent of those selected across ecosystems. Within-species variations of light-related traits are related to demographic responses, linking biotic selection of individuals within communities to eco-evolutionary dynamics of species.

Theranostic Trigger-Responsive Carbon Monoxide-Generating Microbubbles.

Carbon monoxide (CO) is a gaseous signaling molecule that modulates inflammation, cell survival, and recovery after myocardial infarction. However, handling and dosing of CO as a compressed gas are difficult. Here, light-triggerable and magnetic resonance imaging (MRI)-detectable CO release from dimanganese decacarbonyl (CORM-1) are demonstrated, and the development of CORM-1-loaded polymeric microbubbles (COMB) is described as an ultrasound (US)- and MRI-imageable drug delivery platform for triggerable and targeted CO therapy. COMB are synthesized via a straightforward one-step loading protocol, present a narrow size distribution peaking at 2 µm, and show excellent performance as a CORM-1 carrier and US contrast agent. Light irradiation of COMB induces local production and release of CO, as well as enhanced longitudinal and transversal relaxation rates, enabling MRI monitoring of CO delivery. Proof-of-concept studies for COMB-enabled light-triggered CO release show saturation of hemoglobin with CO in human blood, anti-inflammatory differentiation of macrophages, reduction of hypoxia-induced reactive oxygen species (ROS) production, and inhibition of ischemia-induced apoptosis in endothelial cells and cardiomyocytes. These findings indicate that CO-generating MB are interesting theranostic tools for attenuating hypoxia-associated and ROS-mediated cell and tissue damage in cardiovascular disease.

Fire disturbance effects on plant taxonomic and functional ß-diversity mediated by topographic exposure.

Although the diversity-disturbance relationship has been extensively studied, the differences in responses of taxonomic vs. functional diversity to natural disturbances (i.e., fire) call for an improved understanding of this relationship. Here, we investigated how fire disturbance influenced plant taxonomic and functional diversity in Golestan National Park, in northeastern Iran. We evaluated the response of α- and ß-plant diversity considering both taxonomic and functional diversity and different ß-diversity components (i.e., turnover and nestedness) as a function of fire regime, topographic exposure, and their interactive effect. We considered different indices of functional diversity including functional richness, functional evenness, functional divergence, functional dispersion, Rao's quadratic entropy, and community-weighted mean (CWM). Functional diversity indices were computed using four leaf traits related to species growth strategy and fire response including leaf thickness and leaf length, specific leaf area (SLA) and leaf dry matter content (LDMC). Taxonomic and functional diversity had contrasting response to fire disturbance. Fire significantly decreased taxonomic α-diversity similarly in both north and south exposures. ß-diversity increased in south exposures but decreased in north exposures. Fire decreased functional richness, increased CWM of SLA, and decreased CWM of LDMC. In contrast, abundance-weighted metrics of functional diversity (functional evenness, functional divergence, functional dispersion, Rao's quadratic entropy) were not impacted by fire disturbance. Finally, the main contributors to heterogeneity were driven by a fire × exposure interaction, suggesting that fire disturbance interacts with topographic exposure. Our results suggest that taxonomic and functional α- and ß-diversity have contrasting responses to fire illustrating the need to consider both dimensions to understand how disturbance impacts plant communities. At large spatial scale, species turnover and nestedness appear as essential parameters to maintain species-rich communities in response to fire disturbance.

Unveiling ecological assembly rules from commonalities in trait distributions.

Deciphering the effect of neutral and deterministic processes on community assembly is critical to understand and predict diversity patterns. The information held in community trait distributions is commonly assumed as a signature of these processes, but empirical and modelling attempts have most often failed to untangle their confounding, sometimes opposing, impacts. Here, we simulated the assembly of trait distributions through stochastic (dispersal limitation) and/or deterministic scenarios (environmental filtering and niche differentiation). We characterized the shape of trait distributions using the skewness-kurtosis relationship. We identified commonalities in the co-variation between the skewness and the kurtosis of trait distributions with a unique signature for each simulated assembly scenario. Our findings were robust to variation in the composition of regional species pools, dispersal limitation and environmental conditions. While ecological communities can exhibit a high degree of idiosyncrasy, identification of commonalities across multiple communities can help to unveil ecological assembly rules in real-world ecosystems.

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.

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.

Grassland-to-crop conversion in agricultural landscapes has lasting impact on the trait diversity of bees.

CONTEXT: Global pollinator decline has motivated much research to understand the underlying mechanisms. Among the multiple pressures threatening pollinators, habitat loss has been suggested as a key-contributing factor. While habitat destruction is often associated with immediate negative impacts, pollinators can also exhibit delayed responses over time. OBJECTIVES: We used a trait-based approach to investigate how past and current land use at both local and landscape levels impact plant and wild bee communities in grasslands through a functional lens. METHODS: We measured flower and bee morphological traits that mediate plant-bee trophic linkage in 66 grasslands. Using an extensive database of 20 years of land-use records, we tested the legacy effects of the landscape-level conversion of grassland to crop on flower and bee trait diversity. RESULTS: Land-use history was a strong driver of flower and bee trait diversity in grasslands. Particularly, bee trait diversity was lower in landscapes where much of the land was converted from grassland to crop long ago. Bee trait diversity was also strongly driven by plant trait diversity computed with flower traits. However, this relationship was not observed in landscapes with a long history of grassland-to-crop conversion. The effects of land-use history on bee communities were as strong as those of current land use, such as grassland or mass-flowering crop cover in the landscape. CONCLUSIONS: Habitat loss that occurred long ago in agricultural landscapes alters the relationship between plants and bees over time. The retention of permanent grassland sanctuaries within intensive agricultural landscapes can offset bee decline.

Global ecosystem thresholds driven by aridity.

Aridity, which is increasing worldwide because of climate change, affects the structure and functioning of dryland ecosystems. Whether aridification leads to gradual (versus abrupt) and systemic (versus specific) ecosystem changes is largely unknown. We investigated how 20 structural and functional ecosystem attributes respond to aridity in global drylands. Aridification led to systemic and abrupt changes in multiple ecosystem attributes. These changes occurred sequentially in three phases characterized by abrupt decays in plant productivity, soil fertility, and plant cover and richness at aridity values of 0.54, 0.7, and 0.8, respectively. More than 20% of the terrestrial surface will cross one or several of these thresholds by 2100, which calls for immediate actions to minimize the negative impacts of aridification on essential ecosystem services for the more than 2 billion people living in drylands.

Land-use history impacts functional diversity across multiple trophic groups.

Land-use change is a major driver of biodiversity loss worldwide. Although biodiversity often shows a delayed response to land-use change, previous studies have typically focused on a narrow range of current landscape factors and have largely ignored the role of land-use history in shaping plant and animal communities and their functional characteristics. Here, we used a unique database of 220,000 land-use records to investigate how 20-y of land-use changes have affected functional diversity across multiple trophic groups (primary producers, mutualists, herbivores, invertebrate predators, and vertebrate predators) in 75 grassland fields with a broad range of land-use histories. The effects of land-use history on multitrophic trait diversity were as strong as other drivers known to impact biodiversity, e.g., grassland management and current landscape composition. The diversity of animal mobility and resource-acquisition traits was lower in landscapes where much of the land had been historically converted from grassland to crop. In contrast, functional biodiversity was higher in landscapes containing old permanent grasslands, most likely because they offer a stable and high-quality habitat refuge for species with low mobility and specialized feeding niches. Our study shows that grassland-to-crop conversion has long-lasting impacts on the functional biodiversity of agricultural ecosystems. Accordingly, land-use legacy effects must be considered in conservation programs aiming to protect agricultural biodiversity. In particular, the retention of permanent grassland sanctuaries within intensive landscapes may offset ecological debts.

Increasing crop heterogeneity enhances multitrophic diversity across agricultural regions.

Agricultural landscape homogenization has detrimental effects on biodiversity and key ecosystem services. Increasing agricultural landscape heterogeneity by increasing seminatural cover can help to mitigate biodiversity loss. However, the amount of seminatural cover is generally low and difficult to increase in many intensively managed agricultural landscapes. We hypothesized that increasing the heterogeneity of the crop mosaic itself (hereafter "crop heterogeneity") can also have positive effects on biodiversity. In 8 contrasting regions of Europe and North America, we selected 435 landscapes along independent gradients of crop diversity and mean field size. Within each landscape, we selected 3 sampling sites in 1, 2, or 3 crop types. We sampled 7 taxa (plants, bees, butterflies, hoverflies, carabids, spiders, and birds) and calculated a synthetic index of multitrophic diversity at the landscape level. Increasing crop heterogeneity was more beneficial for multitrophic diversity than increasing seminatural cover. For instance, the effect of decreasing mean field size from 5 to 2.8 ha was as strong as the effect of increasing seminatural cover from 0.5 to 11%. Decreasing mean field size benefited multitrophic diversity even in the absence of seminatural vegetation between fields. Increasing the number of crop types sampled had a positive effect on landscape-level multitrophic diversity. However, the effect of increasing crop diversity in the landscape surrounding fields sampled depended on the amount of seminatural cover. Our study provides large-scale, multitrophic, cross-regional evidence that increasing crop heterogeneity can be an effective way to increase biodiversity in agricultural landscapes without taking land out of agricultural production.

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.

Intransitivity increases plant functional diversity by limiting dominance in drylands worldwide.

1. Biotic interactions are key determinants of plant community structure. Indirect interactions such as intransitivity (i.e. in the absence of competitive hierarchies among species) have been hypothesized to benefit diversity within plant communities. However, their effect on functional diversity remains scarcely explored in real communities. Here we develop a novel approach to infer intransitivity from plant spatial patterns and functional traits (height and specific leaf area), and quantify its effect on different components of plant diversity along environmental gradients in 100 drylands from all continents except Antarctica. 2. We first calculated the spatial association pattern for all perennials to infer competition between species. Trait values were used as a proxy of competitive hierarchies to infer the direction of these interactions. We used multiple regression models to evaluate how intransitivity responds to environmental variables (mean annual temperature and precipitation, precipitation seasonality, soil pH, sand content and woody cover). We also used confirmatory path analysis to evaluate the effects of intransitivity on species richness and evenness, trait dispersion and functional diversity. 3. Intransitivity mostly responded to climatic variables, and significantly increased with precipitation scarcity and seasonality. We found that intransitivity had significant effects on functional diversity, mostly by promoting plant community evenness. However, the dominance of woody vegetation (steppes vs. shrublands) modulated this effect. SYNTHESIS: Intransitivity increased the functional diversity of drylands, particularly under high rainfall seasonality, by limiting functionally dominant species. Our findings specify how intransitivity structures the functional diversity of dryland vegetation worldwide. Intransitivity may be particularly important in ecosystems where the availability of abiotic resources changes over time, thereby breaking down inherent competitive hierarchies between plant species. Neglecting intransitivity will bias our estimation of the impacts of biotic interactions on plant communities, a fundamental issue to fully understand how plant communities will respond to ongoing environmental changes.

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.

Description of long-term monitoring of farmland biodiversity in a LTSER.

Understanding the response of biodiversity to management, land use and climate change is a major challenge in farmland to halt the decline of biodiversity. Farmlands shelter a wide variety of taxa, which vary in their life cycle and habitat niches. Consequently, monitoring biodiversity from sessile annual plants to migratory birds requires dedicated protocols. In this article, we describe the protocols applied in a long-term research platform, the LTSER Zone Atelier "Plaine & Val de Sèvre" (for a full description see Bretagnolle et al. (2018) [1]). We present the data in the form of the description of monitoring protocols, which has evolved through time for arable weeds, grassland plants, ground beetles, spiders, grasshoppers, wild bees, hoverflies, butterflies, small mammals, and farmland birds (passerines, owls and various flagship species).

Climate mediates the biodiversity-ecosystem stability relationship globally.

The insurance hypothesis, stating that biodiversity can increase ecosystem stability, has received wide research and political attention. Recent experiments suggest that climate change can impact how plant diversity influences ecosystem stability, but most evidence of the biodiversity-stability relationship obtained to date comes from local studies performed under a limited set of climatic conditions. Here, we investigate how climate mediates the relationships between plant (taxonomical and functional) diversity and ecosystem stability across the globe. To do so, we coupled 14 years of temporal remote sensing measurements of plant biomass with field surveys of diversity in 123 dryland ecosystems from all continents except Antarctica. Across a wide range of climatic and soil conditions, plant species pools, and locations, we were able to explain 73% of variation in ecosystem stability, measured as the ratio of the temporal mean biomass to the SD. The positive role of plant diversity on ecosystem stability was as important as that of climatic and soil factors. However, we also found a strong climate dependency of the biodiversity-ecosystem stability relationship across our global aridity gradient. Our findings suggest that the diversity of leaf traits may drive ecosystem stability at low aridity levels, whereas species richness may have a greater stabilizing role under the most arid conditions evaluated. Our study highlights that to minimize variations in the temporal delivery of ecosystem services related to plant biomass, functional and taxonomic plant diversity should be particularly promoted under low and high aridity conditions, respectively.