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.

Fast-slow traits predict competition network structure and its response to resources and enemies.

Plants interact in complex networks but how network structure depends on resources, natural enemies and species resource-use strategy remains poorly understood. Here, we quantified competition networks among 18 plants varying in fast-slow strategy, by testing how increased nutrient availability and reduced foliar pathogens affected intra- and inter-specific interactions. Our results show that nitrogen and pathogens altered several aspects of network structure, often in unexpected ways due to fast and slow growing species responding differently. Nitrogen addition increased competition asymmetry in slow growing networks, as expected, but decreased it in fast growing networks. Pathogen reduction made networks more even and less skewed because pathogens targeted weaker competitors. Surprisingly, pathogens and nitrogen dampened each other's effect. Our results show that plant growth strategy is key to understand how competition respond to resources and enemies, a prediction from classic theories which has rarely been tested by linking functional traits to competition networks.

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.

Land-use intensity alters networks between biodiversity, ecosystem functions, and services.

Land-use intensification can increase provisioning ecosystem services, such as food and timber production, but it also drives changes in ecosystem functioning and biodiversity loss, which may ultimately compromise human wellbeing. To understand how changes in land-use intensity affect the relationships between biodiversity, ecosystem functions, and services, we built networks from correlations between the species richness of 16 trophic groups, 10 ecosystem functions, and 15 ecosystem services. We evaluated how the properties of these networks varied across land-use intensity gradients for 150 forests and 150 grasslands. Land-use intensity significantly affected network structure in both habitats. Changes in connectance were larger in forests, while changes in modularity and evenness were more evident in grasslands. Our results show that increasing land-use intensity leads to more homogeneous networks with less integration within modules in both habitats, driven by the belowground compartment in grasslands, while forest responses to land management were more complex. Land-use intensity strongly altered hub identity and module composition in both habitats, showing that the positive correlations of provisioning services with biodiversity and ecosystem functions found at low land-use intensity levels, decline at higher intensity levels. Our approach provides a comprehensive view of the relationships between multiple components of biodiversity, ecosystem functions, and ecosystem services and how they respond to land use. This can be used to identify overall changes in the ecosystem, to derive mechanistic hypotheses, and it can be readily applied to further global change drivers.

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.

Plant species-area relationships are determined by evenness, cover and aggregation in drylands worldwide.

AIM: Species-area relationships (also known as 'species-area curves' and 'species accumulation curves') represent the relationship between species richness and the area sampled in a given community. These relationships can be used to describe diversity patterns while accounting for the well-known scale-dependence of species richness. Despite their value, their functional form and parameters, as well as their determinants, have barely been investigated in drylands. LOCATION: 171 drylands from all continents except Antarctica. TIME PERIOD: 2006-2013. MAJOR TAXA STUDIED: Perennial plants. METHODS: We characterized species-area relationships of plant communities by building accumulation curves describing the expected number of species as a function of the number of sampling units, and later compared the fit of three functions (power-law, logarithmic and Michaelis-Menten). We tested the prediction that the effects of aridity, soil pH on SAR are mediated by vegetation attributes such as evenness, cover, and spatial aggregation. RESULTS: We found that the logarithmic relationship was the most common functional form (c.50%), followed by Michaelis-Menten (c.33%) and power-law (c.17%). Functional form was mainly determined by evenness. Power-law relationships were found mostly under low evenness, logarithmic relationships peaked under intermediate evenness and the Michalis-Menten function increased in frequency with increasing evenness. The SAR parameters approximated by the logarithmic model ('small-scale richness' (b0 ) and 'accumulation coefficient' (b1 )) were determined by vegetation attributes. Increasing spatial aggregation had a negative effect on the small-scale richness and a positive effect on the accumulation coefficient, while evenness had an opposite effect. In addition, accumulation coefficient was positively affected by cover. Interestingly, aridity decreased small scale richness but did not affect the accumulation coefficient. MAIN CONCLUSIONS: Our findings highlight the role of evenness, spatial aggregation and cover as main drivers of species area relationships in drylands, the Earth's largest biome.

Synchronization unveils the organization of ecological networks with positive and negative interactions.

Network science has helped to understand the organization principles of the interactions among the constituents of large complex systems. However, recently, the high resolution of the data sets collected has allowed to capture the different types of interactions coexisting within the same system. A particularly important example is that of systems with positive and negative interactions, a usual feature appearing in social, neural, and ecological systems. The interplay of links of opposite sign presents natural difficulties for generalizing typical concepts and tools applied to unsigned networks and, moreover, poses some questions intrinsic to the signed nature of the network, such as how are negative interactions balanced by positive ones so to allow the coexistence and survival of competitors/foes within the same system? Here, we show that synchronization phenomenon is an ideal benchmark for uncovering such balance and, as a byproduct, to assess which nodes play a critical role in the overall organization of the system. We illustrate our findings with the analysis of synthetic and real ecological networks in which facilitation and competitive interactions coexist.

Co-Occurrence Patterns Do Not Predict Mutualistic Interactions Between Plant and Butterfly Species.

Biotic interactions are crucial for determining the structure and dynamics of communities; however, direct measurement of these interactions can be challenging in terms of time and resources, especially when numerous species are involved. Inferring species interactions from species co-occurrence patterns is increasingly being used; however, recent studies have highlighted some limitations. To our knowledge, no attempt has been made to test the accuracy of the existing methods for detecting mutualistic interactions in terrestrial ecosystems. In this study, we compiled two literature-based, long-term datasets of interactions between butterflies and herbaceous plant species in two regions of Germany and compared them with observational abundance and presence/absence data collected within a year in the same regions. We tested how well the species associations generated by three different co-occurrence analysis methods matched those of empirically measured mutualistic associations using sensitivity and specificity analyses and compared the strength of associations. We also checked whether flower abundance data (instead of plant abundance data) increased the accuracy of the co-occurrence models and validated our results using empirical flower visitation data. The results revealed that, although all methods exhibited low sensitivity, our implementation of the Relative Interaction Intensity index with pairwise null models performed the best, followed by the probabilistic method and Spearman's rank correlation method. However, empirical data showed a significant number of interactions that were not detected using co-occurrence methods. Incorporating flower abundance data did not improve sensitivity but enhanced specificity in one region. Further analysis demonstrated incongruence between the predicted co-occurrence associations and actual interaction strengths, with many pairs exhibiting high interaction strength but low co-occurrence or vice versa. These findings underscore the complexity of ecological dynamics and highlight the limitations of current co-occurrence methods for accurately capturing species interactions.

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.

The supply of multiple ecosystem services requires biodiversity across spatial scales.

The impact of local biodiversity loss on ecosystem functioning is well established, but the role of larger-scale biodiversity dynamics in the delivery of ecosystem services remains poorly understood. Here we address this gap using a comprehensive dataset describing the supply of 16 cultural, regulating and provisioning ecosystem services in 150 European agricultural grassland plots, and detailed multi-scale data on land use and plant diversity. After controlling for land-use and abiotic factors, we show that both plot-level and surrounding plant diversity play an important role in the supply of cultural and aboveground regulating ecosystem services. In contrast, provisioning and belowground regulating ecosystem services are more strongly driven by field-level management and abiotic factors. Structural equation models revealed that surrounding plant diversity promotes ecosystem services both directly, probably by fostering the spill-over of ecosystem service providers from surrounding areas, and indirectly, by maintaining plot-level diversity. By influencing the ecosystem services that local stakeholders prioritized, biodiversity at different scales was also shown to positively influence a wide range of stakeholder groups. These results provide a comprehensive picture of which ecosystem services rely most strongly on biodiversity, and the respective scales of biodiversity that drive these services. This key information is required for the upscaling of biodiversity-ecosystem service relationships, and the informed management of biodiversity within agricultural landscapes.

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.

Direct and Indirect Effects of Management Intensity and Environmental Factors on the Functional Diversity of Lichens in Central European Forests.

Using 642 forest plots from three regions in Germany, we analyzed the direct and indirect effects of forest management intensity and of environmental variables on lichen functional diversity (FDis). Environmental stand variables were affected by management intensity and acted as an environmental filter: summing direct and indirect effects resulted in a negative total effect of conifer cover on FDis, and a positive total effect of deadwood cover and standing tree biomass. Management intensity had a direct positive effect on FDis, which was compensated by an indirect negative effect via reduced standing tree biomass and lichen species richness, resulting in a negative total effect on FDis and the FDis of adaptation-related traits (FDisAd). This indicates environmental filtering of management and stronger niche partitioning at a lower intensity. In contrast, management intensity had a positive total effect on the FDis of reproduction-, dispersal- and establishment-related traits (FDisRe), mainly because of the direct negative effect of species richness, indicating functional over-redundancy, i.e., most species cluster into a few over-represented functional entities. Our findings have important implications for forest management: high lichen functional diversity can be conserved by promoting old, site-typical deciduous forests with a high richness of woody species and large deadwood quantity.

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.

Aridity and reduced soil micronutrient availability in global drylands.

Drylands cover more than 40% of terrestrial surface, and their global extent and socio-ecological importance will increase in the future due to the forecasted increases in aridity driven by climate change. Despite the essential role of metallic micronutrients in life chemistry and ecosystem functioning, it is virtually unknown how their bioavailability changes along aridity gradients at the global scale. Here we analysed soil total and available Cu, Fe, Mn, and Zn in 143 drylands from all continents, except Antarctica, covering a broad range of aridity and soil conditions. We found that total and available micronutrient concentrations in dryland soils were low compared to averages commonly found in soils of natural and agricultural ecosystems globally. Aridity negatively affected the availability of all micronutrients evaluated, mainly indirectly by increasing soil pH and decreasing soil organic matter. Remarkably, the available Fe:Zn ratio decreased exponentially as aridity increased, pointing to stoichiometric alterations. Our findings suggest that increased aridity conditions due to climate change will limit the availability of essential micronutrients for organisms, particularly that of Fe and Zn, which together with other adverse effects (e.g., reduced water availability) may pose serious threats to key ecological processes and services, such as food production, in drylands 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.

The structure of plant spatial association networks is linked to plant diversity in global drylands.

1. Despite commonly used to unveil the complex structure of interactions within ecological communities and their value to assess their resilience against external disturbances, network analyses have seldom been applied in plant communities. We evaluated how plant-plant spatial association networks vary in global drylands, and assessed whether network structure was related to plant diversity in these ecosystems. 2. We surveyed 185 dryland ecosystems from all continents except Antarctica and built networks using the local spatial association between all the perennial plants species present in the communities studied. Then, for each network we calculated four descriptors of network structure (link density, link weight mean and heterogeneity, and structural balance), and evaluated their significance with null models. Finally, we used structural equation models to evaluate how abiotic factors (including geography, topography, climate and soil conditions) and network descriptors influenced plant species richness and evenness. 3. Plant networks were highly variable worldwide, but at most study sites (72%) presented common structures such as a higher link density than expected. We also find evidence of the presence of high structural balance in the networks studied. Moreover, all network descriptors considered had a positive and significant effect on plant diversity, and on species richness in particular. Synthesis. Our results constitute the first empirical evidence showing the existence of common network architectures structuring dryland plant communities at the global scale, and suggest a relationship between the structure of spatial networks and plant diversity. They also highlight the importance of system-level approaches to explain the diversity and structure of interactions in plant communities, two major drivers of terrestrial ecosystem functioning.

Evidence for chemical interference effect of an allelopathic plant on neighboring plant species: A field study.

Many studies have reported the phytotoxicity of allelopathic compounds under controlled conditions. However, more field studies are required to provide realistic evidences for the significance of allelopathic interference in natural communities. We conducted a 2-years field experiment in a semiarid plant community (NE Spain). Specifically, we planted juvenile individuals and sowed seeds of Salsola vermiculata L., Lygeum spartum L. and Artemisia herba-alba Asso. (three co-dominant species in the community) beneath adult individuals of the allelopathic shrub A. herba-alba, and assessed the growth, vitality, seed germination and seedling survival of those target species with and without the presence of chemical interference by the incorporation of activated carbon (AC) to the soil. In addition, juveniles and seeds of the same three target species were planted and sown beneath the canopy of adults of S. vermiculata (a shrub similar to A. herba-alba, but non-allelopathic) and in open bare soil to evaluate whether the allelopathic activity of A. herba-alba modulates the net outcome of its interactions with neighboring plants under contrasting abiotic stress conditions. We found that vitality of A. herba-alba juveniles was enhanced beneath A. herba-alba individuals when AC was present. Furthermore, we found that the interaction outcome in A. herba-alba microsite was neutral, whereas a positive outcome was found for S. vermiculata microsite, suggesting that allelopathy may limit the potential facilitative effects of the enhanced microclimatic conditions in A. herba-alba microsite. Yet, L. spartum juveniles were facilitated in A. herba-alba microsite. The interaction outcome in A. herba-alba microsite was positive under conditions of very high abiotic stress, indicating that facilitative interactions predominated over the interference of allelopathic plants under those conditions. These results highlight that laboratory studies can overestimate the significance of allelopathy in nature, and consequently, results obtained under controlled conditions should be interpreted carefully.

Plant-plant interactions as a mechanism structuring plant diversity in a Mediterranean semi-arid ecosystem.

Plant-plant interactions are among the fundamental processes that shape structure and functioning of arid and semi-arid plant communities. Despite the large amount of studies that have assessed the relationship between plant-plant interactions (i.e., facilitation and competition) and diversity, often researchers forget a third kind of interaction, known as allelopathy. We examined the effect of plant-plant interactions of three dominant species: the perennial grass Lygeum spartum, the allelopathic dwarf shrub Artemisia herba-alba, and the nurse shrub Salsola vermiculata, on plant diversity and species composition in a semi-arid ecosystem in NE Spain. Specifically, we quantified the interaction outcome (IO) based on species co-occurrence, we analyzed diversity by calculation of the individual species-area relationship (ISAR), and compositional changes by calculation of the Chao-Jaccard similarity index. We found that S. vermiculata had more positive IO values than L. spartum, and A. herba-alba had values between them. Lygeum spartum and A. herba-alba acted as diversity repellers, whereas S. vermiculata acted as a diversity accumulator. As aridity increased, A. herba-alba transitioned from diversity repeller to neutral and S. vermiculata transitioned from neutral to diversity accumulator, while L. spartum remained as diversity repeller. Artemisia herba-alba had more perennial grass species in its local neighborhood than expected by the null model, suggesting some tolerance of this group to its "chemical neighbor". Consequently, species that coexist with A. herba-alba were very similar among different A. herba-alba individuals. Our findings highlight the role of the nurse shrub S. vermiculata as ecosystem engineer, creating and maintaining patches of diversity, as well as the complex mechanism that an allelopathic plant may have on diversity and species assemblage. Further research is needed to determine the relative importance of allelopathy and competition in the overall interference of allelopathic plants.