Global Ecology Unit CREAF-CSIC-UAB

Elemental stoichiometry constitutes an inherent link between biogeochemistry and the structure and processes within food webs, and thus is at the core of ecosystem functioning. Stoichiometry allows for spanning different levels of biological organization, from cellular metabolism to ecosystem structure and nutrient cycling, and is therefore particularly useful for establishing links between different ecosystem compartments. We review elemental carbon : nitrogen : phosphorus (C:N:P) ratios in terrestrial ecosystems (from vegetation, leaf litter, woody debris, and dead roots, to soil microbes and organic matter). While the stoichiometry of the plant, litter, and soil compartments of ecosystems is well understood, heterotrophic microbial communities, which dominate the soil food web and drive nutrient cycling, have received increasing interest in recent years. This review highlights the effects of resource stoichiometry on soil microorganisms and decomposition, specifically on the structure and function of heterotrophic microbial communities and suggests several general patterns. First, latitudinal gradients of soil and litter stoichiometry are reflected in microbial community structure and function. Second, resource stoichiometry may cause changes in microbial interactions and community dynamics that lead to feedbacks in nutrient availability. Third, global change alters the C:N, C:P, and N:P ratios of primary producers, with repercussions for microbial decomposer communities and critical ecosystem services such as soil fertility. We argue that ecological stoichiometry provides a framework to analyze and predict such global change effects at various scales.

Antibiotic resistance genes (ARGs) have accelerated microbial threats to human health in the last decade. Many genes can confer resistance, but evaluating the relative health risks of ARGs is complex. Factors such as the abundance, propensity for lateral transmission and ability of ARGs to be expressed in pathogens are all important. Here, an analysis at the metagenomic level from various habitats (6 types of habitats, 4572 samples) detects 2561 ARGs that collectively conferred resistance to 24 classes of antibiotics. We quantitatively evaluate the health risk to humans, defined as the risk that ARGs will confound the clinical treatment for pathogens, of these 2561 ARGs by integrating human accessibility, mobility, pathogenicity and clinical availability. Our results demonstrate that 23.78% of the ARGs pose a health risk, especially those which confer multidrug resistance. We also calculate the antibiotic resistance risks of all samples in four main habitats, and with machine learning, successfully map the antibiotic resistance threats in global marine habitats with over 75% accuracy. Our novel method for quantitatively surveilling the health risk of ARGs will help to manage one of the most important threats to human and animal health.

A decline in the carbon fertilization effect One source of uncertainty in climate science is how the carbon fertilization effect (CFE) will contribute to mitigation of anthropogenic climate change. Wang et al. explored the temporal dynamics of CFE on vegetation photosynthesis at the global scale. There has been a decline over recent decades in the contribution of CFE to vegetation photosynthesis, perhaps owing to the limiting effects of plant nutrients such as nitrogen and phosphorus. This declining trend has not been adequately accounted for in carbon cycle models. CFE thus has limitations for long-term mitigation of climate change, and future warming might currently be underestimated. Science , this issue p. 1295

Abstract China’s goal to achieve carbon (C) neutrality by 2060 requires scaling up photovoltaic (PV) and wind power from 1 to 10–15 PWh year −1 (refs. 1–5 ). Following the historical rates of renewable installation 1 , a recent high-resolution energy-system model 6 and forecasts based on China’s 14th Five-year Energy Development (CFED) 7 , however, only indicate that the capacity will reach 5–9.5 PWh year −1 by 2060. Here we show that, by individually optimizing the deployment of 3,844 new utility-scale PV and wind power plants coordinated with ultra-high-voltage (UHV) transmission and energy storage and accounting for power-load flexibility and learning dynamics, the capacity of PV and wind power can be increased from 9 PWh year −1 (corresponding to the CFED path) to 15 PWh year −1 , accompanied by a reduction in the average abatement cost from US$97 to US$6 per tonne of carbon dioxide (tCO 2 ). To achieve this, annualized investment in PV and wind power should ramp up from US$77 billion in 2020 (current level) to US$127 billion in the 2020s and further to US$426 billion year −1 in the 2050s. The large-scale deployment of PV and wind power increases income for residents in the poorest regions as co-benefits. Our results highlight the importance of upgrading power systems by building energy storage, expanding transmission capacity and adjusting power load at the demand side to reduce the economic cost of deploying PV and wind power to achieve carbon neutrality in China.

Abstract Aim Potassium ( K ) is the second most abundant nutrient in plant photosynthetic tissues after nitrogen ( N ). Thousands of physiological and metabolic studies in recent decades have established the fundamental role of K in plant function, especially in water‐use efficiency and economy, and yet macroecological studies have mostly overlooked this nutrient. Methods We have reviewed available studies on the content, stoichiometry and roles of K in the soil–plant system and in terrestrial ecosystems. We have also reviewed the impacts of global change drivers on K content, stoichiometry and roles. Conclusions The current literature indicates that K , at a global level, is as limiting as N and phosphorus ( P ) for plant productivity in terrestrial ecosystems. Some degree of K limitation has been seen in up to 70% of all studied terrestrial ecosystems. However, in some areas atmospheric K deposition from human activities is greater than that from natural sources. We are far from understanding the K fluxes between the atmosphere and land, and the role of anthropogenic activities in these fluxes. The increasing aridity expected in wide areas of the world makes K more critical through its role in water‐use efficiency. N deposition exerts a strong impact on the ecosystem K cycle, decreasing K availability and increasing K limitation. Plant invasive success is enhanced by higher soil K availability, especially in environments without strong abiotic stresses. The impacts of other drivers of global change, such as increasing atmospheric CO 2 or changes in land use, remain to be elucidated. Current models of the responses of ecosystems and carbon storage to projected global climatic and atmospheric changes are now starting to consider N and P , but they should also consider K , mostly in arid and semi‐arid ecosystems.

Potassium, mostly as a cation (K+), together with calcium (Ca2+) are the most abundant inorganic chemicals in plant cellular media, but they are rarely discussed. K+ is not a component of molecular or macromolecular plant structures, thus it is more difficult to link it to concrete metabolic pathways than nitrogen or phosphorus. Over the last two decades, many studies have reported on the role of K+ in several physiological functions, including controlling cellular growth and wood formation, xylem–phloem water content and movement, nutrient and metabolite transport, and stress responses. In this paper, we present an overview of contemporary findings associating K+ with various plant functions, emphasizing plant-mediated responses to environmental abiotic and biotic shifts and stresses by controlling transmembrane potentials and water, nutrient, and metabolite transport. These essential roles of K+ account for its high concentrations in the most active plant organs, such as leaves, and are consistent with the increasing number of ecological and agricultural studies that report K+ as a key element in the function and structure of terrestrial ecosystems, crop production, and global food security. We synthesized these roles from an integrated perspective, considering the metabolic and physiological functions of individual plants and their complex roles in terrestrial ecosystem functions and food security within the current context of ongoing global change. Thus, we provide a bridge between studies of K+ at the plant and ecological levels to ultimately claim that K+ should be considered at least at a level similar to N and P in terrestrial ecological studies.

Numerous studies have demonstrated that fertilization with nutrients such as nitrogen, phosphorus, and potassium increases plant productivity in both natural and managed ecosystems, demonstrating that primary productivity is nutrient limited in most terrestrial ecosystems. In contrast, it has been demonstrated that heterotrophic microbial communities in soil are primarily limited by organic carbon or energy. While this concept of contrasting limitations, that is, microbial carbon and plant nutrient limitation, is based on strong evidence that we review in this paper, it is often ignored in discussions of ecosystem response to global environment changes. The plant-centric perspective has equated plant nutrient limitations with those of whole ecosystems, thereby ignoring the important role of the heterotrophs responsible for soil decomposition in driving ecosystem carbon storage. To truly integrate carbon and nutrient cycles in ecosystem science, we must account for the fact that while plant productivity may be nutrient limited, the secondary productivity by heterotrophic communities is inherently carbon limited. Ecosystem carbon cycling integrates the independent physiological responses of its individual components, as well as tightly coupled exchanges between autotrophs and heterotrophs. To the extent that the interacting autotrophic and heterotrophic processes are controlled by organisms that are limited by nutrient versus carbon accessibility, respectively, we propose that ecosystems by definition cannot be 'limited' by nutrients or carbon alone. Here, we outline how models aimed at predicting non-steady state ecosystem responses over time can benefit from dissecting ecosystems into the organismal components and their inherent limitations to better represent plant-microbe interactions in coupled carbon and nutrient models.

Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species.

Abstract Land use policies have turned southern China into one of the most intensively managed forest regions in the world, with actions maximizing forest cover on soils with marginal agricultural potential while concurrently increasing livelihoods and mitigating climate change. Based on satellite observations, here we show that diverse land use changes in southern China have increased standing aboveground carbon stocks by 0.11 ± 0.05 Pg C y −1 during 2002–2017. Most of this regional carbon sink was contributed by newly established forests (32%), while forests already existing contributed 24%. Forest growth in harvested forest areas contributed 16% and non-forest areas contributed 28% to the carbon sink, while timber harvest was tripled. Soil moisture declined significantly in 8% of the area. We demonstrate that land management in southern China has been removing an amount of carbon equivalent to 33% of regional fossil CO 2 emissions during the last 6 years, but forest growth saturation, land competition for food production and soil-water depletion challenge the longevity of this carbon sink service.

Earlier vegetation greening under climate change raises evapotranspiration and thus lowers spring soil moisture, yet the extent and magnitude of this water deficit persistence into the following summer remain elusive. We provide observational evidence that increased foliage cover over the Northern Hemisphere, during 1982-2011, triggers an additional soil moisture deficit that is further carried over into summer. Climate model simulations independently support this and attribute the driving process to be larger increases in evapotranspiration than in precipitation. This extra soil drying is projected to amplify the frequency and intensity of summer heatwaves. Most feedbacks operate locally, except for a notable teleconnection where extra moisture transpired over Europe is transported to central Siberia. Model results illustrate that this teleconnection offsets Siberian soil moisture losses from local spring greening. Our results highlight that climate change adaptation planning must account for the extra summer water and heatwave stress inherited from warming-induced earlier greening.

Abstract Soil phosphatase levels strongly control the biotic pathways of phosphorus (P), an essential element for life, which is often limiting in terrestrial ecosystems. We investigated the influence of climatic and soil traits on phosphatase activity in terrestrial systems using metadata analysis from published studies. This is the first analysis of global measurements of phosphatase in natural soils. Our results suggest that organic P (P org ), rather than available P, is the most important P fraction in predicting phosphatase activity. Structural equation modeling using soil total nitrogen (TN), mean annual precipitation, mean annual temperature, thermal amplitude and total soil carbon as most available predictor variables explained up to 50% of the spatial variance in phosphatase activity. In this analysis, P org could not be tested and among the rest of available variables, TN was the most important factor explaining the observed spatial gradients in phosphatase activity. On the other hand, phosphatase activity was also found to be associated with climatic conditions and soil type across different biomes worldwide. The close association among different predictors like P org , TN and precipitation suggest that P recycling is driven by a broad scale pattern of ecosystem productivity capacity.

Abstract Question Are plant traits more closely correlated with mean annual temperature, or with mean annual precipitation? Location Global. Methods We quantified the strength of the relationships between temperature and precipitation and 21 plant traits from 447,961 species‐site combinations worldwide. We used meta‐analysis to provide an overall answer to our question. Results Mean annual temperature was significantly more strongly correlated with plant traits than was mean annual precipitation. Conclusions Our study provides support for some of the assumptions of classical vegetation theory, and points to many interesting directions for future research. The relatively low R 2 values for precipitation might reflect the weak link between mean annual precipitation and the availability of water to plants.

Leaf senescence in winter deciduous species signals the transition from the active to the dormant stage. The purpose of leaf senescence is the recovery of nutrients before the leaves fall. Photoperiod and temperature are the main cues controlling leaf senescence in winter deciduous species, with water stress imposing an additional influence. Photoperiod exerts a strict control on leaf senescence at latitudes where winters are severe and temperature gains importance in the regulation as winters become less severe. On average, climatic warming will delay and drought will advance leaf senescence, but at varying degrees depending on the species. Warming and drought thus have opposite effects on the phenology of leaf senescence, and the impact of climate change will therefore depend on the relative importance of each factor in specific regions. Warming is not expected to have a strong impact on nutrient proficiency although a slower speed of leaf senescence induced by warming could facilitate a more efficient nutrient resorption. Nutrient resorption is less efficient when the leaves senesce prematurely as a consequence of water stress. The overall effects of climate change on nutrient resorption will depend on the contrasting effects of warming and drought. Changes in nutrient resorption and proficiency will impact production in the following year, at least in early spring, because the construction of new foliage relies almost exclusively on nutrients resorbed from foliage during the preceding leaf fall. Changes in the phenology of leaf senescence will thus impact carbon uptake, but also ecosystem nutrient cycling, especially if the changes are consequence of water stress.

MOTIVATION: The BioTIME database contains raw data on species identities and abundances in ecological assemblages through time. These data enable users to calculate temporal trends in biodiversity within and amongst assemblages using a broad range of metrics. BioTIME is being developed as a community-led open-source database of biodiversity time series. Our goal is to accelerate and facilitate quantitative analysis of temporal patterns of biodiversity in the Anthropocene. MAIN TYPES OF VARIABLES INCLUDED: The database contains 8,777,413 species abundance records, from assemblages consistently sampled for a minimum of 2 years, which need not necessarily be consecutive. In addition, the database contains metadata relating to sampling methodology and contextual information about each record. SPATIAL LOCATION AND GRAIN: ). TIME PERIOD AND GRAIN: BioTIME records span from 1874 to 2016. The minimal temporal grain across all datasets in BioTIME is a year. MAJOR TAXA AND LEVEL OF MEASUREMENT: BioTIME includes data from 44,440 species across the plant and animal kingdoms, ranging from plants, plankton and terrestrial invertebrates to small and large vertebrates. SOFTWARE FORMAT: .csv and .SQL.

BACKGROUND: Plant phenology has crucial biological, physical, and chemical effects on the biosphere. Phenological drivers have largely been studied, but the role of plant microbiota, particularly rhizosphere microbiota, has not been considered. RESULTS: We discovered that rhizosphere microbial communities could modulate the timing of flowering of Arabidopsis thaliana. Rhizosphere microorganisms that increased and prolonged N bioavailability by nitrification delayed flowering by converting tryptophan to the phytohormone indole acetic acid (IAA), thus downregulating genes that trigger flowering, and stimulating further plant growth. The addition of IAA to hydroponic cultures confirmed this metabolic network. CONCLUSIONS: We document a novel metabolic network in which soil microbiota influenced plant flowering time, thus shedding light on the key role of soil microbiota on plant functioning. This opens up multiple opportunities for application, from helping to mitigate some of the effects of climate change and environmental stress on plants (e.g. abnormal temperature variation, drought, salinity) to manipulating plant characteristics using microbial inocula to increase crop potential.

Root exudates comprise a large variety of compounds released by plants into the rhizosphere, including low-molecular-weight primary metabolites (particularly saccharides, amino acids and organic acids) and secondary metabolites (phenolics, flavonoids and terpenoids). Changes in exudate composition could have impacts on the plant itself, on other plants, on soil properties (e.g. amount of soil organic matter), and on soil organisms. The effects of drought on the composition of root exudates, however, have been rarely studied. We used an ecometabolomics approach to identify the compounds in the exudates of Quercus ilex (holm oak) under an experimental drought gradient and subsequent recovery. Increasing drought stress strongly affected the composition of the exudate metabolome. Plant exudates under drought consisted mainly of secondary metabolites (71% of total metabolites) associated with plant responses to drought stress, whereas the metabolite composition under recovery shifted towards a dominance of primary metabolites (81% of total metabolites). These results strongly suggested that roots exude the most abundant root metabolites. The exudates were changed irreversibly by the lack of water under extreme drought conditions, and the plants could not recover.

Terrestrial primary productivity and carbon cycle impacts of droughts are commonly quantified using vapour pressure deficit (VPD) data and remotely sensed greenness, without accounting for soil moisture. However, soil moisture limitation is known to strongly affect plant physiology. Here, we investigate light use efficiency, the ratio of gross primary productivity (GPP) to absorbed light. We derive its fractional reduction due to soil moisture (fLUE), separated from VPD and greenness changes, using artificial neural networks trained on eddy covariance data, multiple soil moisture datasets and remotely sensed greenness. This reveals substantial impacts of soil moisture alone that reduce GPP by up to 40% at sites located in sub-humid, semi-arid or arid regions. For sites in relatively moist climates, we find, paradoxically, a muted fLUE response to drying soil, but reduced fLUE under wet conditions. fLUE identifies substantial drought impacts that are not captured when relying solely on VPD and greenness changes and, when seasonally recurring, are missed by traditional, anomaly-based drought indices. Counter to common assumptions, fLUE reductions are largest in drought-deciduous vegetation, including grasslands. Our results highlight the necessity to account for soil moisture limitation in terrestrial primary productivity data products, especially for drought-related assessments.

Vegetation in water-limited ecosystems relies strongly on access to deep water reserves to withstand dry periods. Most of these ecosystems have shallow soils over deep groundwater reserves. Understanding the functioning and functional plasticity of species-specific root systems and the patterns of or differences in the use of water sources under more frequent or intense droughts is therefore necessary to properly predict the responses of seasonally dry ecosystems to future climate. We used stable isotopes to investigate the seasonal patterns of water uptake by a sclerophyll forest on sloped terrain with shallow soils. We assessed the effect of a long-term experimental drought (12 years) and the added impact of an extreme natural drought that produced widespread tree mortality and crown defoliation. The dominant species, Quercus ilex, Arbutus unedo and Phillyrea latifolia, all have dimorphic root systems enabling them to access different water sources in space and time. The plants extracted water mainly from the soil in the cold and wet seasons but increased their use of groundwater during the summer drought. Interestingly, the plants subjected to the long-term experimental drought shifted water uptake toward deeper (10-35 cm) soil layers during the wet season and reduced groundwater uptake in summer, indicating plasticity in the functional distribution of fine roots that dampened the effect of our experimental drought over the long term. An extreme drought in 2011, however, further reduced the contribution of deep soil layers and groundwater to transpiration, which resulted in greater crown defoliation in the drought-affected plants. This study suggests that extreme droughts aggravate moderate but persistent drier conditions (simulated by our manipulation) and may lead to the depletion of water from groundwater reservoirs and weathered bedrock, threatening the preservation of these Mediterranean ecosystems in their current structures and compositions.

Abstract The massive use of fertilizers during the last decades allowed a great increase in the global capacity of food production. However, in the last years, several studies highlight the inefficiency and country asymmetries in the use of these fertilizers that generated environmental problems, soil nutritional imbalances and not optimal food production. We have aimed to summarize this information and identify and disentangle the key caveats that should be solved. Inadequate global management of fertilization produces areas with serious nutrient deficits in croplands linked with insufficient access to fertilizers that clearly limit food production, and areas that are overfertilized with the consequent problems of environmental pollution affecting human health. A more efficient use of nitrogen (N), phosphorus (P) and potassium (K) fertilizers for food security while preserving the environment is thus needed. Nutrient imbalances, particularly the disequilibrium of the N:P ratio due to the unbalanced release of N and P from anthropogenic activities, mainly by crop fertilization and expanding N-fixing crops that have continuously increased the soil N:P ratio, is another issue to resolve. This imbalance has already affected several terrestrial and aquatic ecosystems, altering their species composition and functionality and threatening global biodiversity. The different economic and geopolitical traits of these three main macronutrient fertilizers must be considered. P has the fewest reserves, depending mostly on mineable efforts, with most of the reserves concentrated in very few countries (85% in Morocco). This problem is a great concern for the current and near-future access to P for low-income countries. N is instead readily available due to the well-established and relatively low-cost Haber–Bosch synthesis of ammonium from atmospheric N 2 , which is increasingly used, even in some low-income countries producing an increasing imbalance in nutrient ratios with the application of P and K fertilizers. The anthropogenic inputs of these three macronutrients to the environment have reached the levels of the natural fluxes, thereby substantially altering their global cycles. The case of the excess of N fertilization is especially paradigmatic in several areas of the world, where continental water sources have become useless due to the higher nitrate concentrations. The management of N, P and K fertilizers is thus in the center of the main dichotomy between food security and environmentally driven problems, such as climate change or eutrophication/pollution. Such a key role demands new legislation for adopting the well-known and common-sense 4R principle (right nutrient source at the right rate, right time and right place) that would help to ensure the appropriate use of nutrient resources and the optimization of productivity.

Plant functional traits can predict community assembly and ecosystem functioning and are thus widely used in global models of vegetation dynamics and land-climate feedbacks. Still, we lack a global understanding of how land and climate affect plant traits. A previous global analysis of six traits observed two main axes of variation: (1) size variation at the organ and plant level and (2) leaf economics balancing leaf persistence against plant growth potential. The orthogonality of these two axes suggests they are differently influenced by environmental drivers. We find that these axes persist in a global dataset of 17 traits across more than 20,000 species. We find a dominant joint effect of climate and soil on trait variation. Additional independent climate effects are also observed across most traits, whereas independent soil effects are almost exclusively observed for economics traits. Variation in size traits correlates well with a latitudinal gradient related to water or energy limitation. In contrast, variation in economics traits is better explained by interactions of climate with soil fertility. These findings have the potential to improve our understanding of biodiversity patterns and our predictions of climate change impacts on biogeochemical cycles.