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Optimal stomatal theory predicts that stomata operate to maximise photosynthesis (Anet) and minimise transpirational water loss to achieve optimal intrinsic water-use efficiency (iWUE). We tested whether this theory can predict stomatal responses to elevated atmospheric CO2 (eCO2), and whether it can capture differences in responsiveness among woody plant functional types (PFTs). We conducted a meta-analysis of tree studies of the effect of eCO2 on iWUE and its components Anet and stomatal conductance (gs). We compared three PFTs, using the unified stomatal optimisation (USO) model to account for confounding effects of leaf–air vapour pressure difference (D). We expected smaller gs, but greater Anet, responses to eCO2 in gymnosperms compared with angiosperm PFTs. We found that iWUE increased in proportion to increasing eCO2 in all PFTs, and that increases in Anet had stronger effects than reductions in gs. The USO model correctly captured stomatal behaviour with eCO2 across most datasets. The chief difference among PFTs was a lower stomatal slope parameter (g1) for the gymnosperm, compared with angiosperm, species. Land surface models can use the USO model to describe stomatal behaviour under changing atmospheric CO2 conditions. AG gratefully acknowledges a studentship provided by the John Horseman Trust and the University of Birmingham. The BIFoR FACE facility is supported by the JABBS Foundation, the University of Birmingham and the John Horseman Trust. ARMK acknowledges support from the UK Natural Environment Research Council through grant NE/S015833/1. MJ and BEM acknowledge funding from the Australian Research Council (DE210101654, FL190100003).

Plant responses to elevated atmospheric carbon dioxide (eCO2 ) have been hypothesized as a key mechanism that may ameliorate the impact of future drought. Yet, despite decades of experiments, the question of whether eCO2 reduces plant water use, yielding 'water savings' that can be used to maintain plant function during periods of water stress, remains unresolved. In this Viewpoint, we identify the experimental challenges and limitations to our understanding of plant responses to drought under eCO2 . In particular, we argue that future studies need to move beyond exploring whether eCO2 played 'a role' or 'no role' in responses to drought, but instead more carefully consider the timescales and conditions that would induce an influence. We also argue that considering emergent differences in soil water content may be an insufficient means of assessing the impact of eCO2 . We identify eCO2 impact during severe drought (e.g. to the point of mortality), interactions with future changes in vapour pressure deficit and uncertainty about changes in leaf area as key gaps in our current understanding. New insights into CO2 × drought interactions are essential to better constrain model theory that governs future climate model projections of land-atmosphere interactions during periods of water stress.

Eastern Australia was subject to its hottest and driest year on record in 2019. This extreme drought resulted in massive canopy die-back in eucalypt forests. The role of hydraulic failure and tree size on canopy die-back in three eucalypt tree species during this drought was examined. We measured pre-dawn and midday leaf water potential (Ψleaf ), per cent loss of stem hydraulic conductivity and quantified hydraulic vulnerability to drought-induced xylem embolism. Tree size and tree health was also surveyed. Trees with most, or all, of their foliage dead exhibited high rates of native embolism (78-100%). This is in contrast to trees with partial canopy die-back (30-70% canopy die-back: 72-78% native embolism), or relatively healthy trees (little evidence of canopy die-back: 25-31% native embolism). Midday Ψleaf was significantly more negative in trees exhibiting partial canopy die-back (-2.7 to -6.3 MPa), compared with relatively healthy trees (-2.1 to -4.5 MPa). In two of the species the majority of individuals showing complete canopy die-back were in the small size classes. Our results indicate that hydraulic failure is strongly associated with canopy die-back during drought in eucalypt forests. Our study provides valuable field data to help constrain models predicting mortality risk.

Elevated atmospheric CO2 (eCa ) may benefit plants during drought by reducing stomatal conductance (gs ) but any 'water savings effect' could be neutralized by concurrent stimulation of leaf area. We investigated whether eCa enhanced water savings, thereby ameliorating the impact of drought on carbon and water relations in trees. We report leaf-level gas exchange and whole-plant and soil water relations during a short-term dry-down in two Eucalyptus species with contrasting drought tolerance. Plants had previously been established for 9 to 11 months in steady-state conditions of ambient atmospheric CO2 (aCa ) and eCa , with half of each treatment group exposed to sustained drought for 5 to 7 months. The lower stomatal conductance under eCa did not lead to soil moisture savings during the dry-down due to the counteractive effect of increased whole-plant leaf area. Nonetheless, eCa -grown plants maintained higher photosynthetic rates and leaf water potentials, making them less stressed during the dry-down, despite being larger. These effects were more pronounced in the xeric species than the mesic species, and in previously water-stressed plants. Our findings indicate that eCa may enhance plant performance during drought despite a lack of soil water savings, especially in species with more conservative growth and water-use strategies.

The classical theory of stomatal optimization stipulates that stomata should act to maximize photosynthesis while minimizing transpiration. This theory, despite its remarkable success in reproducing empirical patterns, does not account for the fact that the available water to plants is dynamically regulated by plants themselves, and that plants compete for water in most locations. Here, we develop an alternative theory in which plants maximize the expected carbon gain under stochastic rainfall in a competitive environment. We further incorporate xylem hydraulic limitation as an additional constraint to transpiration and evaluate its impacts on stomatal optimization by incorporating the direct carbon cost of xylem recovery and the opportunity cost of reduced future photosynthesis as a result of irrecoverable xylem damage. We predict stomatal behaviour to be more conservative with a higher cost induced by xylem damage. By varying the unit carbon cost and extent of xylem recovery, characterizing the direct and opportunity cost of xylem damage, respectively, our model can reproduce several key patterns of stomatal-hydraulic trait covariations. By addressing the key elements of water limitation in plant gas exchange simultaneously, including plants' self-regulation of water availability, competition for water and hydraulic risk, our study provides a comprehensive theoretical basis for understanding stomatal behaviour.

© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust The ratio of leaf intercellular to ambient CO 2 (χ) is modulated by stomatal conductance (g s ). These quantities link carbon (C) assimilation with transpiration, and along with photosynthetic capacities (V cmax and J max ) are required to model terrestrial C uptake. We use optimization criteria based on the growth environment to generate predicted values of photosynthetic and water-use efficiency traits and test these against a unique dataset. Leaf gas-exchange parameters and carbon isotope discrimination were analysed in relation to local climate across a continental network of study sites. Sun-exposed leaves of 50 species at seven sites were measured in contrasting seasons. Values of χ predicted from growth temperature and vapour pressure deficit were closely correlated to ratios derived from C isotope (δ 13 C) measurements. Correlations were stronger in the growing season. Predicted values of photosynthetic traits, including carboxylation capacity (V cmax ), derived from δ 13 C, growth temperature and solar radiation, showed meaningful agreement with inferred values derived from gas-exchange measurements. Between-site differences in water-use efficiency were, however, only weakly linked to the plant's growth environment and did not show seasonal variation. These results support the general hypothesis that many key parameters required by Earth system models are adaptive and predictable from plants’ growth environments.

Summary Models of tree responses to climate typically project that elevated atmospheric CO2 concentration (eCa) will reduce drought impacts on forests. We tested one of the mechanisms underlying this interaction, the ‘low Ci effect’, in which stomatal closure in drought conditions reduces the intercellular CO2 concentration (Ci), resulting in a larger relative enhancement of photosynthesis with eCa, and, consequently, a larger relative biomass response. We grew two Eucalyptus species of contrasting drought tolerance at ambient and elevated Ca for 6–9 months in large pots maintained at 50% (drought) and 100% field capacity. Droughted plants did not have significantly lower Ci than well-watered plants, which we attributed to long-term changes in leaf area. Hence, there should not have been an interaction between eCa and water availability on biomass, and we did not detect one. The xeric species did have higher Ci than the mesic species, indicating lower water-use efficiency, but both species exhibited similar responses of photosynthesis and biomass to eCa, owing to compensatory differences in the photosynthetic response to Ci. Our results demonstrate that long-term acclimation to drought, and coordination among species traits may be important for predicting plant responses to eCa under low water availability.

The first generation of forest free-air CO2 enrichment (FACE) experiments has successfully provided deeper understanding about how forests respond to an increasing CO2 concentration in the atmosphere. Located in aggrading stands in the temperate zone, they have provided a strong foundation for testing critical assumptions in terrestrial biosphere models that are being used to project future interactions between forest productivity and the atmosphere, despite the limited inference space of these experiments with regards to the range of global ecosystems. Now, a new generation of FACE experiments in mature forests in different biomes and over a wide range of climate space and biodiversity will significantly expand the inference space. These new experiments are: EucFACE in a mature Eucalyptus stand on highly weathered soil in subtropical Australia; AmazonFACE in a highly diverse, primary rainforest in Brazil; BIFoR-FACE in a 150-yr-old deciduous woodland stand in central England; and SwedFACE proposed in a hemiboreal, Pinus sylvestris stand in Sweden. We now have a unique opportunity to initiate a model-data interaction as an integral part of experimental design and to address a set of cross-site science questions on topics including responses of mature forests; interactions with temperature, water stress, and phosphorus limitation; and the influence of biodiversity.

The sensitivity of photosynthetic metabolism to temperature has been identified as a key uncertainty for projecting the magnitude of the terrestrial feedback on future climate change. While temperature responses of photosynthetic capacities have been comparatively well investigated in temperate species, the responses of tropical tree species remain unexplored. We compared the responses of seedlings of native cold-adapted tropical montane rainforest tree species with those of exotic warm-adapted plantation species, all growing in an intermediate temperature common garden in Rwanda. Leaf gas exchange responses to carbon dioxide (CO2 ) at different temperatures (20-40°C) were used to assess the temperature responses of biochemical photosynthetic capacities. Analyses revealed a lower optimum temperature for photosynthetic electron transport rates than for Rubisco carboxylation rates, along with lower electron transport optima in the native cold-adapted than in the exotic warm-adapted species. The photosynthetic optimum temperatures were generally exceeded by daytime peak leaf temperatures, in particular in the native montane rainforest climax species. This study thus provides evidence of pronounced negative effects of high temperature in tropical trees and indicates high susceptibility of montane rainforest climax species to future global warming.

Summary Approximately 1–2% of net primary production by land plants is re-emitted to the atmosphere as isoprene and monoterpenes. These emissions play major roles in atmospheric chemistry and air pollution–climate interactions. Phenomenological models have been developed to predict their emission rates, but limited understanding of the function and regulation of these emissions has led to large uncertainties in model projections of air quality and greenhouse gas concentrations. We synthesize recent advances in diverse fields, from cell physiology to atmospheric remote sensing, and use this information to propose a simple conceptual model of volatile isoprenoid emission based on regulation of metabolism in the chloroplast. This may provide a robust foundation for scaling up emissions from the cellular to the global scale.

We analysed the responses of 11 ecosystem models to elevated atmospheric [CO2] (eCO(2)) at two temperate forest ecosystems (Duke and Oak Ridge National Laboratory (ORNL) Free-Air CO2 Enrichment (FACE) experiments) to test alternative representations of carbon (C)-nitrogen (N) cycle processes. We decomposed the model responses into component processes affecting the response to eCO(2) and confronted these with observations from the FACE experiments. Most of the models reproduced the observed initial enhancement of net primary production (NPP) at both sites, but none was able to simulate both the sustained 10-yr enhancement at Duke and the declining response at ORNL: models generally showed signs of progressive N limitation as a result of lower than observed plant N uptake. Nonetheless, many models showed qualitative agreement with observed component processes. The results suggest that improved representation of above-ground-below-ground interactions and better constraints on plant stoichiometry are important for a predictive understanding of eCO(2) effects. Improved accuracy of soil organic matter inventories is pivotal to reduce uncertainty in the observed C-N budgets. The two FACE experiments are insufficient to fully constrain terrestrial responses to eCO(2), given the complexity of factors leading to the observed diverging trends, and the consequential inability of the models to explain these trends. Nevertheless, the ecosystem models were able to capture important features of the experiments, lending some support to their projections. (Less)

• Data from 13 long-term (> 1 yr), field-based studies of the effects of elevated CO2 concentration ([CO2]) on European forest tree species were analysed using meta-analysis and modelling. Meta-analysis was used to determine mean responses across the data sets, and data were fitted to two commonly used models of stomatal conductance in order to explore response to environmental conditions and the relationship with assimilation. • Meta-analysis indicated a significant decrease (21%) in stomatal conductance in response to growth in elevated [CO2] across all studies. The response to [CO2] was significantly stronger in young trees than old trees, in deciduous compared to coniferous trees, and in water stressed compared to nutrient stressed trees. No evidence of acclimation of stomatal conductance to elevated [CO2] was found. • Fits of data to the first model showed that growth in elevated [CO2] did not alter the response of stomatal conductance to vapour pressure deficit, soil water content or atmospheric [CO2]. Fits of data to the second model indicated that conductance and assimilation responded in parallel to elevated [CO2] except when water was limiting. • Data were compared to a previous meta-analysis and it was found that the response of gs to elevated [CO2] was much more consistent in long-term (> 1 yr) studies, emphasising the need for long-term elevated [CO2] studies. By interpreting data in terms of models, the synthesis will aid future modelling studies of responses of forest trees to elevated [CO2].