Chlorophyll fluorescence variation in two Mediterranean forest species over a 21-year drought treatment period.

The Mediterranean is among the regions predicted to be most affected by climate change due to rising temperatures and increasing frequency as well as intensity of extreme weather events, such as drought. These shifts in climatic conditions might lead to changes in species community composition by enabling the increase of drought-tolerant species at the expense of less tolerant ones. This hypothesis was tested in the current study using chlorophyll fluorescence data from a 21-year precipitation exclusion experiment in a Mediterranean forest for two co-dominant Quercus ilex L. and Phillyrea latifolia L. species with contrasting low and high levels of drought tolerance, respectively. The maximum potential quantum efficiency of photosystem II (PSII) (Fv/Fm), photochemical efficiency of PSII (yield) and non-photochemical quenching (NPQ) varied seasonally. The Fv/Fm and NPQ levels were positively correlated with air temperature and standardized precipitation-evapotranspiration index (SPEI), whereas yield, which was greater under drought treatment, was negatively associated with vapor pressure deficit and SPEI. The Fv/Fm values showed similar increase in the two species over the 21-year study period regardless of treatment and in parallel to progressive warming. By contrast, yield values were higher in Q. ilex than in P. latifolia, while NPQ values were higher in P. latifolia than in Q. ilex. Notably, high yield values were also observed in the drought-treated plots. Throughout the study, plants in the drought-treated plots exhibited decreased basal area, leaf biomass and aerial cover due to high stem mortality. In addition, a continuous increase in temperature was detected in summer and autumn, which might explain the observed increase in Fv/Fm values over the study period. Higher yield and lower NPQ detected in Q. ilex could be attributed to less competition for resources in the drought-treated plots and acclimation of Q. ilex plants over the study period. Our results indicate that reduction in stem density could improve forest resilience to climate change-induced drought conditions.

The essential role of biodiversity in the key axes of ecosystem function.

Biodiversity is essential for maintaining the terrestrial ecosystem multifunctionality (EMF). Recent studies have revealed that the variations in terrestrial ecosystem functions are captured by three key axes: the maximum productivity, water use efficiency, and carbon use efficiency of the ecosystem. However, the role of biodiversity in supporting these three key axes has not yet been explored. In this study, we combined the (i) data collected from more than 840 vegetation plots across a large climatic gradient in China using standard protocols, (ii) data on plant traits and phylogenetic information for more than 2,500 plant species, and (iii) soil nutrient data measured in each plot. These data were used to systematically assess the contribution of environmental factors, species richness, functional and phylogenetic diversity, and community-weighted mean (CWM) and ecosystem traits (i.e., traits intensity normalized per unit land area) to EMF via hierarchical partitioning and Bayesian structural equation modeling. Multiple biodiversity attributes accounted for 70% of the influence of all the variables on EMF, and ecosystems with high functional diversity had high resource use efficiency. Our study is the first to systematically explore the role of different biodiversity attributes, including species richness, phylogenetic and functional diversity, and CWM and ecosystem traits, in the key axes of ecosystem functions. Our findings underscore that biodiversity conservation is critical for sustaining EMF and ultimately ensuring human well-being.

Diagnosing destabilization risk in global land carbon sinks.

Global net land carbon uptake or net biome production (NBP) has increased during recent decades1. Whether its temporal variability and autocorrelation have changed during this period, however, remains elusive, even though an increase in both could indicate an increased potential for a destabilized carbon sink2,3. Here, we investigate the trends and controls of net terrestrial carbon uptake and its temporal variability and autocorrelation from 1981 to 2018 using two atmospheric-inversion models, the amplitude of the seasonal cycle of atmospheric CO2 concentration derived from nine monitoring stations distributed across the Pacific Ocean and dynamic global vegetation models. We find that annual NBP and its interdecadal variability increased globally whereas temporal autocorrelation decreased. We observe a separation of regions characterized by increasingly variable NBP, associated with warm regions and increasingly variable temperatures, lower and weaker positive trends in NBP and regions where NBP became stronger and less variable. Plant species richness presented a concave-down parabolic spatial relationship with NBP and its variability at the global scale whereas nitrogen deposition generally increased NBP. Increasing temperature and its increasing variability appear as the most important drivers of declining and increasingly variable NBP. Our results show increasing variability of NBP regionally that can be mostly attributed to climate change and that may point to destabilization of the coupled carbon-climate system.

MASTREE+: Time-series of plant reproductive effort from six continents.

Significant gaps remain in understanding the response of plant reproduction to environmental change. This is partly because measuring reproduction in long-lived plants requires direct observation over many years and such datasets have rarely been made publicly available. Here we introduce MASTREE+, a data set that collates reproductive time-series data from across the globe and makes these data freely available to the community. MASTREE+ includes 73,828 georeferenced observations of annual reproduction (e.g. seed and fruit counts) in perennial plant populations worldwide. These observations consist of 5971 population-level time-series from 974 species in 66 countries. The mean and median time-series length is 12.4 and 10 years respectively, and the data set includes 1122 series that extend over at least two decades (≥20 years of observations). For a subset of well-studied species, MASTREE+ includes extensive replication of time-series across geographical and climatic gradients. Here we describe the open-access data set, available as a.csv file, and we introduce an associated web-based app for data exploration. MASTREE+ will provide the basis for improved understanding of the response of long-lived plant reproduction to environmental change. Additionally, MASTREE+ will enable investigation of the ecology and evolution of reproductive strategies in perennial plants, and the role of plant reproduction as a driver of ecosystem dynamics.

Aún existen importantes vacíos en la comprensión de la respuesta reproductiva de las plantas al cambio medioambiental, en parte, porque su monitoreo en especies de plantas longevas requiere una observación directa durante muchos años, y estos conjuntos de datos rara vez han estado disponibles. Aquí presentamos a MASTREE +, una base de datos que recopila series de tiempo de la reproducción de las plantas de todo el planeta, poniendo a disposición estos datos de libre acceso para la comunidad científica. MASTREE + incluye 73.828 puntos de observación de la reproducción anual georreferenciados (ej. conteos de semillas y frutos) en poblaciones de plantas perennes en todo el mundo. Estas observaciones consisten en 5971 series temporales a nivel de población provenientes de 974 especies en 66 países. La mediana de la duración de las series de tiempo es de 10 años (media = 12.4 años) y el conjunto de datos incluye 1.122 series de al menos dos décadas (≥20 años de observaciones). Para un subconjunto de especies bien estudiadas, MASTREE +incluye un amplio conjunto de series temporales replicadas en gradientes geográficos y climáticos. Describimos el conjunto de datos de acceso abierto disponible como un archivo.csv y presentamos una aplicación web asociada para la exploración de datos. MASTREE+ proporcionará la base para mejorar la comprensión sobre la respuesta reproductiva de plantas longevas al cambio medioambiental. Además, MASTREE+ facilitará los avances en la investigación de la ecología y la evolución de las estrategias reproductivas en plantas perennes y el papel de la reproducción vegetal como determinante de la dinámica de ecosistemas.

Global maps and factors driving forest foliar elemental composition: the importance of evolutionary history.

Consistent information on the current elemental composition of vegetation at global scale and the variables that determine it is lacking. To fill this gap, we gathered a total of 30 912 georeferenced records on woody plants foliar concentrations of nitrogen (N), phosphorus (P) and potassium (K) from published databases, and produced global maps of foliar N, P and K concentrations for woody plants using neural networks at a resolution of 1 km2 . We used data for climate, atmospheric deposition, soil and morphoclimatic groups to train the neural networks. Foliar N, P and K do not follow clear global latitudinal patterns but are consistent with the hypothesis of soil substrate age. We additionally built generalized linear mixed models to investigate the evolutionary history effect together with the effects of environmental effects. In this comparison, evolutionary history effects explained most of the variability in all cases (mostly > 60%). These results emphasize the determinant role of evolutionary history in foliar elemental composition, which should be incorporated in upcoming dynamic global vegetation models.

From atoms to ecosystems: elementome diversity meets ecosystem functioning.

The elemental composition of plants (the elementome) is a reliable indicator of their functional traits and the ecological strategies that they follow, and thus represents a good predictor of how ecosystems work. Biodiversity and, especially, functional diversity are also widely recognized as important drivers of ecosystem functioning, mainly because of niche partitioning amongst different species. Here, I review evidence indicating that plant elementomes relate to their ecological niches and how plant elemental concentrations may shift in response to abiotic and biotic drivers. I propose the use of ecosystem elementome diversity as a universal metric to compare ecosystems and investigate diversity-ecosystem functioning relationships. Future research using this promising novel approach will bring together elementomes, diversity, and ecosystem functioning.

The three major axes of terrestrial ecosystem function.

The leaf economics spectrum1,2 and the global spectrum of plant forms and functions3 revealed fundamental axes of variation in plant traits, which represent different ecological strategies that are shaped by the evolutionary development of plant species2. Ecosystem functions depend on environmental conditions and the traits of species that comprise the ecological communities4. However, the axes of variation of ecosystem functions are largely unknown, which limits our understanding of how ecosystems respond as a whole to anthropogenic drivers, climate and environmental variability4,5. Here we derive a set of ecosystem functions6 from a dataset of surface gas exchange measurements across major terrestrial biomes. We find that most of the variability within ecosystem functions (71.8%) is captured by three key axes. The first axis reflects maximum ecosystem productivity and is mostly explained by vegetation structure. The second axis reflects ecosystem water-use strategies and is jointly explained by variation in vegetation height and climate. The third axis, which represents ecosystem carbon-use efficiency, features a gradient related to aridity, and is explained primarily by variation in vegetation structure. We show that two state-of-the-art land surface models reproduce the first and most important axis of ecosystem functions. However, the models tend to simulate more strongly correlated functions than those observed, which limits their ability to accurately predict the full range of responses to environmental changes in carbon, water and energy cycling in terrestrial ecosystems7,8.

Response to Comments on "Recent global decline of CO2 fertilization effects on vegetation photosynthesis".

Our study suggests that the global CO2 fertilization effect (CFE) on vegetation photosynthesis has declined during the past four decades. The Comments suggest that the temporal inconsistency in AVHRR data and the attribution method undermine the results' robustness. Here, we provide additional evidence that these arguments did not affect our finding and that the global decline in CFE is robust.

Do Bryophyte Elemental Concentrations Explain Their Morphological Traits?

Differences in the elemental composition of plants, mainly C, N, and P, have been shown to be related to differences in their nutritional status, and their morphological and functional traits. The relationship between morphological traits and micronutrients and trace elements, however, has been much less studied. Additionally, in bryophytes, research devoted to investigating these relationships is still very scarce. Here, we analysed 80 samples from 29 aquatic and semi-aquatic (hygrophytic) moss species living in Mediterranean springs to investigate the relationship between moss nutrient concentrations and their micro- and macroscopic morphological traits and growth forms. We found that, across species, the elemental concentration of mosses was more tightly linked to macroscopic traits than to microscopic traits. Growth forms could also be successfully explained by the concentration of elements in mosses. Apart from macronutrients and their stoichiometric ratios (C:N, C:P, and N:P), micronutrients and trace elements were also important variables predicting moss morphological traits and growth forms. Additionally, our results showed that microscopic traits were well related to macroscopic traits. Overall, our results clearly indicate that the elemental composition of mosses can be used to infer their morphological traits, and that elements other than macronutrients should be taken into account to achieve a good representation of their morphological and, potentially, functional traits when comparing the elemental composition across species.

The effect of global change on soil phosphatase activity.

Soil phosphatase enzymes are produced by plant roots and microorganisms and play a key role in the cycling of phosphorus (P), an often-limiting element in terrestrial ecosystems. The production of these enzymes in soil is the most important biological strategy for acquiring phosphate ions from organic molecules. Previous works showed how soil potential phosphatase activity is mainly driven by climatic conditions and soil nitrogen (N) and carbon. Nonetheless, future trends of the activity of these enzymes under global change remain little known. We investigated the influence of some of the main drivers of change on soil phosphatase activity using a meta-analysis of results from 97 published studies. Our database included a compilation of N and P fertilization experiments, manipulation experiments with increased atmospheric CO2 concentration, warming, and drought, and studies comparing invaded and non-invaded ecosystems. Our results indicate that N fertilization leads to higher phosphatase activity, whereas P fertilization has the opposite effect. The rise of atmospheric CO2 levels or the arrival of invasive species also exhibits positive response ratios on the activity of soil phosphatases. However, the occurrence of recurrent drought episodes decreases the activity of soil phosphatases. Our analysis did not reveal statistically significant effects of warming on soil phosphatase activity. In general, soil enzymatic changes in the reviewed experiments depended on the initial nutrient and water status of the ecosystems. The observed patterns evidence that future soil phosphatase activity will not only depend on present-day soil conditions but also on potential compensations or amplifications among the different drivers of global change. The responses of soil phosphatases to the global change drivers reported in this study and the consideration of cost-benefit approaches based on the connection of the P and N cycle will be useful for a better estimation of phosphatase production in carbon (C)-N-P models.

Measuring temporal patterns in ecology: The case of mast seeding.

Properly assessing temporal patterns is a central issue in ecology in order to understand ecosystem processes and their mechanisms. Mast seeding has traditionally been described as a reproductive behavior consisting of highly variable and synchronized reproductive events. The most common metric used to measure temporal variability and thus infer masting behavior, the coefficient of variation (CV), however, has been repeatedly suggested to improperly estimate temporal variability. Biases of CV estimates are especially problematic for non-normally distributed data and/or data sets with a high number of zeros.Some recent studies have already adopted new metrics to measure temporal variability, but most continue to use CV. This controversy has started a strong debate about what metrics to use.We here summarize the problems of CV when assessing temporal variability, particularly across data sets containing a large number of zeros, and highlight the benefits of using other metrics of temporal variability, such as proportional variability (PV) and consecutive disparity (D). We also suggest a new way to look at reproductive behavior, by separating temporal variability from frequency of reproduction, to allow better comparison of data sets with different characteristics.We suggest future studies to properly describe the temporal patterns in fully scientific and measurable terms that do not lead to confusion, such as variability and frequency of reproduction, using robust and fully comparable metrics.

Bryophyte C:N:P stoichiometry, biogeochemical niches and elementome plasticity driven by environment and coexistence.

Ecological stoichiometry and studies of biogeochemical niches have mainly focused on plankton and vascular plants, but the phenotypically closest modern relatives of early plants, bryophytes, have been largely neglected. We analysed C:N:P stoichiometries and elemental compositions (K, Na, Mg, Ca, S, Fe) of 35 widely distributed bryophyte species inhabiting springs. We estimated bryophyte C:N:P ratios and their biogeochemical niches, investigated how elementomes respond to the environment and determined whether they tend to diverge more for coexisting than non-coexisting individuals and species. The median C:N:P was 145:8:1, intermediate between Redfield's ratio for marine plankton and those for vascular plants. Biogeochemical niches were differentiated amongst species and were phylogenetically conserved. Differences in individual and species-specific elementomes increased with coexistence between species. Our results provide an evolutionary bridge between the ecological stoichiometries of algae and vascular plants and suggest that differences in elementomes could be used to understand community assemblages and functional diversity.

Increasing climatic sensitivity of global grassland vegetation biomass and species diversity correlates with water availability.

Grasslands are key repositories of biodiversity and carbon storage and are heavily impacted by effects of global warming and changes in precipitation regimes. Patterns of grassland dynamics associated with variability in future climate conditions across spatiotemporal scales are yet to be adequately quantified. Here, we performed a global meta-analysis of year and growing season sensitivities of vegetation aboveground biomass (AGB), aboveground net primary productivity (ANPP), and species richness (SR) and diversity (Shannon index, H) to experimental climate warming and precipitation shifts. All four variables were sensitive to climate change. Their sensitivities to shifts in precipitation were correlated with local background water availability, such as mean annual precipitation (MAP) and aridity, and AGB and ANPP sensitivities were greater in dry habitats than in nonwater-limited habitats. There was no effect of duration of experiment (short vs long term) on sensitivities. Temporal trends in ANPP and SR sensitivity depended on local water availability; ANPP sensitivity to warming increased over time and SR sensitivity to irrigation decreased over time. Our results provide a global overview of the sensitivities of grassland function and diversity to climate change that will improve the understanding of ecological responses across spatiotemporal scales and inform policies for conservation in dry climates.

Empirical support for the biogeochemical niche hypothesis in forest trees.

The possibility of using the elemental compositions of species as a tool to identify species/genotype niche remains to be tested at a global scale. We investigated relationships between the foliar elemental compositions (elementomes) of trees at a global scale with phylogeny, climate, N deposition and soil traits. We analysed foliar N, P, K, Ca, Mg and S concentrations in 23,962 trees of 227 species. Shared ancestry explained 60-94% of the total variance in foliar nutrient concentrations and ratios whereas current climate, atmospheric N deposition and soil type together explained 1-7%, consistent with the biogeochemical niche hypothesis which predicts that each species will have a specific need for and use of each bio-element. The remaining variance was explained by the avoidance of nutritional competition with other species and natural variability within species. The biogeochemical niche hypothesis is thus able to quantify species-specific tree niches and their shifts in response to environmental changes.

Recent leveling off of vegetation greenness and primary production reveals the increasing soil water limitations on the greening Earth.

Global vegetation photosynthesis and productivity have increased substantially since the 1980s, but this trend is heterogeneous in both time and space. Here, we categorize the secular trend in global vegetation greenness into sustained greening, sustained browning and greening-to-browning. We found that by 2016, increased global vegetation greenness had begun to level off, with the area of browning increasing in the last decade, reaching 39.0 million km2 (35.9% of the world's vegetated area). This area is larger than the area with sustained increasing growth (27.8 million km2, 26.4%); thus, 12.0% ± 3.1% (0.019 ± 0.004 NDVI a-1) of the previous earlier increase has been offset since 2010 (2010-2016, P < 0.05). Global gross primary production also leveled off, following the trend in vegetation greenness in time and space. This leveling off was caused by increasing soil water limitations due to the spatial expansion of drought, whose impact dominated over the impacts of temperature and solar radiation. This response of global gross primary production to soil water limitation was not identified by land submodels within Earth system models. Our results provide empirical evidence that global vegetation greenness and primary production are offset by water stress and suggest that as global warming continues, land submodels may overestimate the world's capacity to take up carbon with global vegetation greening.

Recent global decline of CO2 fertilization effects on vegetation photosynthesis.

The enhanced vegetation productivity driven by increased concentrations of carbon dioxide (CO2) [i.e., the CO2 fertilization effect (CFE)] sustains an important negative feedback on climate warming, but the temporal dynamics of CFE remain unclear. Using multiple long-term satellite- and ground-based datasets, we showed that global CFE has declined across most terrestrial regions of the globe from 1982 to 2015, correlating well with changing nutrient concentrations and availability of soil water. Current carbon cycle models also demonstrate a declining CFE trend, albeit one substantially weaker than that from the global observations. This declining trend in the forcing of terrestrial carbon sinks by increasing amounts of atmospheric CO2 implies a weakening negative feedback on the climatic system and increased societal dependence on future strategies to mitigate climate warming.

The role of climate, foliar stoichiometry and plant diversity on ecosystem carbon balance.

Global change is affecting terrestrial carbon (C) balances. The effect of climate on ecosystem C balance has been largely explored, but the roles of other concurrently changing factors, such as diversity and nutrient availability, remain elusive. We used eddy-covariance C-flux measurements from 62 ecosystems from which we compiled information on climate, ecosystem type, stand age, species abundance and foliar concentrations of N and P of the main species, to assess their importance in the ecosystem C balance. Climate and productivity were the main determinants of ecosystem C balance and its stability. In P-rich sites, increasing N was related to increased gross primary production and respiration and vice versa, but reduced net C uptake. Our analyses did not provide evidence for a strong relation between ecosystem diversity and their productivity and stability. Nonetheless, these results suggest that nutrient imbalances and, potentially, diversity loss may alter future global C balance.

Deciphering the Biotic and Climatic Factors That Influence Floral Scents: A Systematic Review of Floral Volatile Emissions.

Currently, a global analysis of the information available on the relative composition of the floral scents of a very diverse variety of plant species is missing. Such analysis may reveal general patterns on the distribution and dominance of the volatile compounds that form these mixtures, and may also allow measuring the effects of factors such as the phylogeny, pollination vectors, and climatic conditions on the floral scents of the species. To fill this gap, we compiled published data on the relative compositions and emission rates of volatile organic compounds (VOCs) in the floral scents of 305 plant species from 66 families. We also gathered information on the groups of pollinators that visited the flowers and the climatic conditions in the areas of distribution of these species. This information allowed us to characterize the occurrence and relative abundances of individual volatiles in floral scents and the effects of biotic and climatic factors on floral scent. The monoterpenes trans-ß-ocimene and linalool and the benzenoid benzaldehyde were the most abundant floral VOCs, in both ubiquity and predominance in the floral blends. Floral VOC richness and relative composition were moderately preserved traits across the phylogeny. The reliance on different pollinator groups and the climate also had important effects on floral VOC richness, composition, and emission rates of the species. Our results support the hypothesis that key compounds or compounds originating from specific biosynthetic pathways mediate the attraction of the main pollinators. Our results also indicate a prevalence of monoterpenes in the floral blends of plants that grow in drier conditions, which could link with the fact that monoterpene emissions protect plants against oxidative stresses throughout drought periods and their emissions are enhanced under moderate drought stress. Sesquiterpenes, in turn, were positively correlated with mean annual temperature, supporting that sesquiterpene emissions are dominated mainly by ambient temperature. This study is the first to quantitatively summarise data on floral-scent emissions and provides new insights into the biotic and climatic factors that influence floral scents.

Is forest fecundity resistant to drought? Results from an 18-yr rainfall-reduction experiment.

Recruitment is a primary determinant of the long-term dynamics of plant populations in changing environments. However, little information is known about the effects of anthropogenic environmental changes on reproductive ecology of trees. We evaluated the impact of experimentally induced 18 yr of drought on reproduction of three contrasting forest trees: Quercus ilex, Phillyrea latifolia and Arbutus unedo. Rainfall reduction did not decrease tree fecundity. Drought, however, affected the allocation of resources in Q. ilex and A. unedo but not the more drought tolerant P. latifolia. Larger crop production by Q. ilex and A. unedo was associated with a stronger decrease in growth in the rainfall-reduction plots compared with the control plots, suggesting that these species were able to maintain their fecundity by shifting their allocation of resources away from growth. Our results indicated resistance to change in tree fecundity in Mediterranean-type forest subjected to an average 15% decrease in the amount of soil moisture, suggesting that these ecosystems may adapt to a progressive increase in arid conditions. However, the species-specific reductions in growth may indirectly affect future fecundity and ultimately shift community composition, even without immediate direct effects of drought on tree fecundity.

Increasing atmospheric CO2 concentrations correlate with declining nutritional status of European forests.

The drivers of global change, including increases in atmospheric CO2 concentrations, N and S deposition, and climate change, likely affect the nutritional status of forests. Here we show forest foliar concentrations of N, P, K, S and Mg decreased significantly in Europe by 5%, 11%, 8%, 6% and 7%, respectively during the last three decades. The decrease in nutritional status was especially large in Mediterranean and temperate forests. Increasing atmospheric CO2 concentration was well correlated with the decreases in N, P, K, Mg, S concentrations and the increase of N:P ratio. Regional analyses indicated that increases in some foliar nutrient concentrations such as N, S and Ca in northern Europe occurred associated with increasingly favourable conditions of mean annual precipitation and temperature. Crucial changes in forest health, structure, functioning and services, including negative feedbacks on C capture can be expected if these trends are not reversed.