Altered activities of extracellular soil enzymes by the interacting global environmental changes.

Soil enzymes are crucial in mediating ecosystems' responses to environmental drivers, so that the comprehension of their sensitivity to drivers of global change can help make predictions of future scenarios and design tailored interventions of biomanipulation. Drivers of global change usually act in combination of two or more, and indirect effects of one driver acting through modification of another one often occur, yet most of both manipulative and meta-analysis studies available tend to focus on the direct effect of one single driver on the activity of specific soil enzymes. One of the biggest challenges is, therefore, represented by the difficulty in assessing the interactions between different drivers, due to the complexity of disentangling the single direct effects from the indirect and combined ones. In this review, after elucidating the general mechanisms of soil enzyme production and activity regulation, we display the state-of-the-art knowledge on direct, indirect and combined effects of the main drivers of global change on soil enzyme activities, identify gaps in knowledge and challenges from research, plus we analyse how this can reverberate in the future of biomanipulation techniques for the improvement of ecosystem services. We conclude that qualitative but not quantitative outcomes can be predicted for some interactions such as warming + drought or warming + CO2 , while for other ones, the results are controversial: future basic research will have to center on this holistic approach. A general trend toward the overall increase of soil enzyme activities and acceleration of biogeochemical cycles will persist, until an inflection will be caused by factors such as future shifts in microbial communities and changes in carbon use efficiency. Applied research will develop toward the refinement of "in situ" analytical systems for the study of soil enzyme activities and the support of bioengineering for the better tailoring of interventions of biomanipulation.

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.

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.

Inter-individual variability in spring phenology of temperate deciduous trees depends on species, tree size and previous year autumn phenology.

We explored the inter-individual variability in bud-burst and its potential drivers, in homogeneous mature stands of temperate deciduous trees. Phenological observations of leaves and wood formation were performed weekly from summer 2017 to summer 2018 for pedunculate oak, European beech and silver birch in Belgium. The variability of bud-burst was correlated to previous' year autumn phenology (i.e. the onset of leaf senescence and the cessation of wood formation) and tree size but with important differences among species. In fact, variability of bud-burst was primarily related to onset of leaf senescence, cessation of wood formation and tree height for oak, beech and birch, respectively. The inter-individual variability of onset of leaf senescence was not related to the tree characteristics considered and was much larger than the inter-individual variability in bud-burst. Multi-species multivariate models could explain up to 66% of the bud-burst variability. These findings represent an important advance in our fundamental understanding and modelling of phenology and tree functioning of deciduous tree species.

Timeline of autumn phenology in temperate deciduous trees.

Cessation of xylem formation or wood growth (CWG) and onset of foliar senescence (OFS) are key autumn phenological events in temperate deciduous trees. Their timing is fundamental for the development and survival of trees, ecosystem nutrient cycling and the seasonal exchange of matter and energy between the biosphere and atmosphere, and affects the impact and feedback of forests to global change. A large-scale experimental effort and improved observational methods have allowed us to compare the timing of CWG and OFS for different deciduous tree species in Western Europe, particularly in silver birch, a pioneer species, and European beech, a late-succession species, at stands of different latitudes, of different levels of site fertility, for 2 years with contrasting meteorological and drought conditions, i.e., the low moderately dry 2017 and the extremely dry 2018. Specifically, we tested whether foliar senescence started before, after or concurrently with CWG. Onset of foliar senescence and CWG occurred generally between late September and early November, with larger differences across species and sites for OFS. Foliar senescence started concurrently with CWG in most cases, except for the drier 2018 and, for beech, at the coldest site, where OFS occurred significantly later than CWG. The behavior of beech in Spain, the southern edge of its European distribution, was unclear, with no CWG, but very low wood growth at the time of OFS. Our study suggests that OFS is generally triggered by the same drivers of CWG or when wood growth decreases in late summer, indicating an overarching mechanism of sink limitation as a possible regulator of the timing of foliar senescence.

Effects of seasonal and decadal warming on soil enzymatic activity in a P-deficient Mediterranean shrubland.

Soil enzymes are central in the response of terrestrial ecosystems to climate change, and their study can be crucial for the models' implementation. We investigated for 1 year the effects of warming and seasonality on the potential activities of five soil extracellular enzymes and their relationships with soil moisture, phosphorus (P) concentration, and other soil parameters in a P-limited Mediterranean semiarid shrubland. The site was continuously subjected to warming since 1999, and we compared data from this study to analogous data from 2004. Warming uniformly increased all enzymes activities, but only when a sufficient amount of soil water was available. Seasonality unevenly altered enzyme activities, thus affecting enzymatic stoichiometry. P deficiency affected enzymatic stoichiometry, favoring the activities of the phosphatases. The effect of warming was stronger in 2014 than 2004, excluding the hypothesis of acclimation of rhizospheric responses to higher temperatures and suggesting that further increases in extracellular enzymatic activities are to be expected if sufficient water is available. Climatic warming will likely generally stimulate soil enzymatic activities and accelerate nutrient mineralization and similar ecological processes such as the production and degradation of biomass and changes in community composition, but which will be limited by water availability, especially in Mediterranean soils in summer. Winters in such ecosystems will benefit from a general increase in activity and production, but biological activity could even decrease in summer, potentially leading to a negative overall balance of nutrient mineralization. This study suggests that a general increase in activity due to warming could lead to faster mineralization of soil organic matter and water consumption in colder climates, until one of these factors in turn becomes limiting. Such trade-offs between water and temperature in relation with enzyme activity should be considered in biogeochemical models.

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.

Tropospheric ozone as a fungal elicitor.

Tropospheric ozone has been proven to trigger biochemical plant responses that are similar to the ones induced by an attack of fungal pathogens,i.e. it resembles fungal elicitors.This suggests that ozone can represent a valid tool for the study of stress responses and induction of resistance to pathogens. This review provides an overview of the implications of such a phenomenon for basic and applied research. After an introduction about the environmental implications of tropospheric ozone and plant responses to biotic stresses, the biochemistry of ozone stress is analysed, pointing out its similarities with plant responses to pathogens and its possible applications.