Victoria Ochoa

Plant species richness and ecosystem multifunctionality in global drylands

Global Ecosystem Analysis The relationship between species richness and the functional properties of their ecosystems has often been studied at small scales in experimental plots. Maestre et al. (p. 214; see the Perspective by Midgley) performed field measurements at 224 dryland sites from six continents and assessed 14 ecosystem functions related to carbon, nitrogen, and phosphorus cycling. Positive relationships were observed between perennial plant species richness and ecosystem functionality. The relative importance of biodiversity was found to be as large as, or larger than, many key abiotic variables. Thus, preservation of plant biodiversity is important to buffer negative effects of climate change and desertification in drylands, which collectively cover 41% of Earths land surface and support over 38% of the human population. Plant species richness is positively related to ecosystem multifunctionality in drylands at a global scale. Experiments suggest that biodiversity enhances the ability of ecosystems to maintain multiple functions, such as carbon storage, productivity, and the buildup of nutrient pools (multifunctionality). However, the relationship between biodiversity and multifunctionality has never been assessed globally in natural ecosystems. We report here on a global empirical study relating plant species richness and abiotic factors to multifunctionality in drylands, which collectively cover 41% of Earth’s land surface and support over 38% of the human population. Multifunctionality was positively and significantly related to species richness. The best-fitting models accounted for over 55% of the variation in multifunctionality and always included species richness as a predictor variable. Our results suggest that the preservation of plant biodiversity is crucial to buffer negative effects of climate change and desertification in drylands.

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.

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.

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

Significance Climate change is increasing the degree of aridity in drylands, which occupy 41% of Earth’s surface and support 38% of its population. Soil bacteria and fungi are largely responsible for key ecosystem services, including soil fertility and climate regulation, yet their responses to changes in aridity are poorly understood. Using a field survey conducted in drylands worldwide and DNA-sequencing approaches, we found that increases in aridity reduce the diversity and abundance of soil bacteria and fungi. This study represents an important advancement in our understanding of soil microbial communities and their likely responses to ongoing climate change. Soil bacteria and fungi play key roles in the functioning of terrestrial ecosystems, yet our understanding of their responses to climate change lags significantly behind that of other organisms. This gap in our understanding is particularly true for drylands, which occupy ∼41% of Earth´s surface, because no global, systematic assessments of the joint diversity of soil bacteria and fungi have been conducted in these environments to date. Here we present results from a study conducted across 80 dryland sites from all continents, except Antarctica, to assess how changes in aridity affect the composition, abundance, and diversity of soil bacteria and fungi. The diversity and abundance of soil bacteria and fungi was reduced as aridity increased. These results were largely driven by the negative impacts of aridity on soil organic carbon content, which positively affected the abundance and diversity of both bacteria and fungi. Aridity promoted shifts in the composition of soil bacteria, with increases in the relative abundance of Chloroflexi and α-Proteobacteria and decreases in Acidobacteria and Verrucomicrobia. Contrary to what has been reported by previous continental and global-scale studies, soil pH was not a major driver of bacterial diversity, and fungal communities were dominated by Ascomycota. Our results fill a critical gap in our understanding of soil microbial communities in terrestrial ecosystems. They suggest that changes in aridity, such as those predicted by climate-change models, may reduce microbial abundance and diversity, a response that will likely impact the provision of key ecosystem services by global drylands.

Differences in thallus chemistry are related to species‐specific effects of biocrust‐forming lichens on soil nutrients and microbial communities

Summary 1. It is well-known that vascular plants have species-specific effects on soil properties. However, little is known on how individual species forming biocrusts, communities dominated by lichens, mosses and cyanobacteria that are prevalent in many ecosystems world-wide, affect microbial communities and soil variables related to nutrient cycling. 2. We evaluated the relationship of six biocrust-forming lichens (Buellia epipolia, Diploschistes diacapsis, Fulgensia subbracteata, Psora decipiens, Squamarina cartilaginea and Squamarina lentigera) with microbial abundance and multiple variables associated with soil nitrogen (N), carbon (C) and phosphorus (P) cycling and storage. We also evaluated whether the composition of lichen tissues (contents in C, N, P and polyphenols) is related to the C, N, P availability and microbial abundance in soils. Finally, we assessed what lichen species positively and negatively relate to soil fertility compared to bare ground areas without biocrusts. 3. We found contrasted C, N, P availability and soil microbial abundance under the different biocrust-forming lichens. Interestingly, inorganic P and amino acids were the most important factors differentiating lichen microsites. These differences in nutrient availability seem to be related to the C, N and P composition of the lichen tissues. For example, soils under D. diacapsis and P. decipiens, which had the lowest and highest C, N and P contents in their tissues, respectively, had the lowest and highest nutrient availability, respectively. We also found contrasted soil microbes abundance under the different soil lichens. For instance, F. subbracteata and D. diacapsis were negatively related to the abundance of bacteria compared to bare ground areas. 4. Our results support the idea that, as found with vascular plants, biocrust-forming lichens have species-specific effects on soil microbial communities and C, N and P cycling. Thus, continuing considering biocrusts as a unique entity will only add confusion to our knowledge of how they control nutrient availability and microbial abundance in the ecosystems where this key community is prevalent.

Simulated climate change reduced the capacity of lichen-dominated biocrusts to act as carbon sinks in two semi-arid Mediterranean ecosystems

The importance of biological soil crusts (biocrusts) for the biogeochemistry of drylands is widely recognized. However, there are significant gaps in our knowledge about how climate change will affect these organisms and the processes depending on them. We conducted a manipulative full factorial experiment in two representative dryland ecosystems from central (Aranjuez) and southeastern (Sorbas) Spain to evaluate how precipitation, temperature and biocrust cover affected the assimilation and net C balance of biocrusts. Chlorophyll fluorescence, net photosynthesis and dark respiration were measured in situ bimonthly during a year. We also conducted daily cycle measurements of net photosynthesis in winter and at the end of spring. In Sorbas, warming reduced the fixation of atmospheric C in biocrust-dominated microsites throughout the year. In Aranjuez, there was an interaction between the three factors evaluated; during winter, net photosynthesis was significantly greater in high biocrust cover plots under natural conditions and in the rainfall exclusion treatment. During the daily surveys, rainfall exclusion and warming reduced C fixation in Sorbas and in Aranjuez respectively. The effects of the treatments evaluated varied with the rainfall and non-rainfall water inputs (NRWIs) registered before the measurements. Our results suggest that changes in NRWI regimes as consequence of warming could have a greater impact on the C balance of biocrusts than changes in rainfall amounts. They also indicate that climate change may reduce the photosynthetic ability of lichens, with a consequent reduction of their dominance in biocrust communities at the mid to long term. This could reduce the ability of dryland ecosystems to fix atmospheric C.

Direct and indirect impacts of climate change on microbial and biocrust communities alter the resistance of the N cycle in a semiarid grassland

Summary 1. Climate change will raise temperatures and modify precipitation patterns in drylands worldwide, affecting their structure and functioning. Despite the recognized importance of soil communities dominated by mosses, lichens and cyanobacteria (biocrusts) as a driver of nutrient cycling in drylands, little is known on how biocrusts will modulate the resistance (i.e., the amount of change caused by a disturbance) of the N cycle in response to climate change. 2. Here, we evaluate how warming (ambient vs. ~2.5 °C increase), rainfall exclusion (ambient vs. ~30% reduction in total annual rainfall) and biocrust cover (incipient vs. well-developed biocrusts) affect multiple variables linked to soil N availability (inorganic and organic N and potential net N mineralization rate) and its resistance to climate change during 4 years in a field experiment. We also evaluate how climate change-induced modifications in biocrust and microbial communities indirectly affect such resistance. 3. Biocrusts promoted the resistance of soil N availability regardless of the climatic conditions considered. However, the dynamics of N availability diverged progressively from their original conditions with warming and/or rainfall exclusion, as both treatments enhanced N availability and promoted the dominance of inorganic over organic N. In addition, the increase in fungal:bacterial ratio and the decrease in biocrust cover observed under warming had a negative indirect effect on the resistance of N cycle variables. 4. Synthesis. Our results indicate that climate change will have negative direct and indirect (i.e. through changes in biocrust and microbial communities) impacts on the resistance of the N cycle in dryland soils. While biocrusts can play an important role slowing down the impacts of climate change on the N cycle due to their positive and continued effects on the resistance of multiple variables from the N cycle, such change will progressively alter N cycling in biocrust-dominated ecosystems, enhancing both N availability and inorganic N dominance.

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.

Climate and soil attributes determine plant species turnover in global drylands

AIM Geographic, climatic, and soil factors are major drivers of plant beta diversity, but their importance for dryland plant communities is poorly known. This study aims to: i) characterize patterns of beta diversity in global drylands, ii) detect common environmental drivers of beta diversity, and iii) test for thresholds in environmental conditions driving potential shifts in plant species composition. LOCATION 224 sites in diverse dryland plant communities from 22 geographical regions in six continents. METHODS Beta diversity was quantified with four complementary measures: the percentage of singletons (species occurring at only one site), Whittakes beta diversity (β(W)), a directional beta diversity metric based on the correlation in species occurrences among spatially contiguous sites (β(R2)), and a multivariate abundance-based metric (β(MV)). We used linear modelling to quantify the relationships between these metrics of beta diversity and geographic, climatic, and soil variables. RESULTS Soil fertility and variability in temperature and rainfall, and to a lesser extent latitude, were the most important environmental predictors of beta diversity. Metrics related to species identity (percentage of singletons and β(W)) were most sensitive to soil fertility, whereas those metrics related to environmental gradients and abundance ((β(R2)) and β(MV)) were more associated with climate variability. Interactions among soil variables, climatic factors, and plant cover were not important determinants of beta diversity. Sites receiving less than 178 mm of annual rainfall differed sharply in species composition from more mesic sites (> 200 mm). MAIN CONCLUSIONS Soil fertility and variability in temperature and rainfall are the most important environmental predictors of variation in plant beta diversity in global drylands. Our results suggest that those sites annually receiving ~ 178 mm of rainfall will be especially sensitive to future climate changes. These findings may help to define appropriate conservation strategies for mitigating effects of climate change on dryland vegetation.

Aridity Modulates N Availability in Arid and Semiarid Mediterranean Grasslands

While much is known about the factors that control each component of the terrestrial nitrogen (N) cycle, it is less clear how these factors affect total N availability, the sum of organic and inorganic forms potentially available to microorganisms and plants. This is particularly true for N-poor ecosystems such as drylands, which are highly sensitive to climate change and desertification processes that can lead to the loss of soil nutrients such as N. We evaluated how different climatic, abiotic, plant and nutrient related factors correlate with N availability in semiarid Stipa tenacissima grasslands along a broad aridity gradient from Spain to Tunisia. Aridity had the strongest relationship with N availability, suggesting the importance of abiotic controls on the N cycle in drylands. Aridity appeared to modulate the effects of pH, plant cover and organic C (OC) on N availability. Our results suggest that N transformation rates, which are largely driven by variations in soil moisture, are not the direct drivers of N availability in the studied grasslands. Rather, the strong relationship between aridity and N availability could be driven by indirect effects that operate over long time scales (decades to millennia), including both biotic (e.g. plant cover) and abiotic (e.g. soil OC and pH). If these factors are in fact more important than short-term effects of precipitation on N transformation rates, then we might expect to observe a lagged decrease in N availability in response to increasing aridity. Nevertheless, our results suggest that the increase in aridity predicted with ongoing climate change will reduce N availability in the Mediterranean basin, impacting plant nutrient uptake and net primary production in semiarid grasslands throughout this region.