Stomatal response to environmental conditions forms the backbone of all ecosystem and carbon cycle models, but is largely based on empirical relationships. Evolutionary theories of stomatal behaviour are critical for guarding against prediction errors of empirical models under future climates. Longstanding theory holds that stomata maximise fitness by acting to maintain constant marginal water use efficiency over a given time horizon, but a recent evolutionary theory proposes that stomata instead maximise carbon gain minus carbon costs/risk of hydraulic damage. Using data from 34 species that span global forest biomes, we find that the recent carbon‐maximisation optimisation theory is widely supported, revealing that the evolution of stomatal regulation has not been primarily driven by attainment of constant marginal water use efficiency. Optimal control of stomata to manage hydraulic risk is likely to have significant consequences for ecosystem fluxes during drought, which is critical given projected intensification of the global hydrological cycle.

Climate change is expected to lead to increases in drought frequency and severity, with deleterious effects on many ecosystems. Stomatal responses to changing environmental conditions form the backbone of all ecosystem models, but are based on empirical relationships and are not well-tested during drought conditions. Here, we use a dataset of 34 woody plant species spanning global forest biomes to examine the effect of leaf water potential on stomatal conductance and test the predictive accuracy of three major stomatal models and a recently proposed model. We find that current leaf-level empirical models have consistent biases of over-prediction of stomatal conductance during dry conditions, particularly at low soil water potentials. Furthermore, the recently proposed stomatal conductance model yields increases in predictive capability compared to current models, and with particular improvement during drought conditions. Our results reveal that including stomatal sensitivity to declining water potential and consequent impairment of plant water transport will improve predictions during drought conditions and show that many biomes contain a diversity of plant stomatal strategies that range from risky to conservative stomatal regulation during water stress. Such improvements in stomatal simulation are greatly needed to help unravel and predict the response of ecosystems to future climate extremes.

Initial growth of germinated seeds is an important life history stage, critical for establishment and succession in forests. Important questions remain regarding the differences among species in early growth potential arising from shade tolerance. In addition, the role of leaf habit in shaping relationships underlying shade tolerance-related differences in seedling growth remains unresolved. In this study we examined variation in morphological and physiological traits among seedlings of 10 forest tree species of the European temperate zone varying in shade tolerance and leaf habit (broadleaved winter-deciduous species vs needle-leaved conifers) during a 10-week period. Seeds were germinated and grown in a controlled environment simulating an intermediate forest understory light environment to resolve species differences in initial growth and biomass allocation. In the high-resource experimental conditions during the study, seedlings increased biomass allocation to roots at the cost of leaf biomass independent of shade tolerance and leaf habit. Strong correlations between relative growth rate (RGR), net assimilation rate (NAR), leaf area ratio (LAR), specific leaf area (SLA) and leaf mass fraction (LMF) indicate that physiology and biomass allocation were equally important determinants of RGR as plant structure and leaf morphology among these species. Our findings highlight the importance of seed mass- and seed size-related root morphology (specific root length—SRL) for shade tolerance during early ontogeny. Leaf and plant morphology (SLA, LAR) were more successful in explaining variation among species due to leaf habit than shade tolerance. In both broadleaves and conifers, shade-tolerant species had lower SRL and greater allocation of biomass to stems (stem mass fraction). Light-seeded shade-intolerant species with greater SRL had greater RGR in both leaf habit groups. However, the greatest plant mass was accumulated in the group of heavy-seeded shade-tolerant broadleaves. The results of our study suggest that the combinations of plant attributes enhancing growth under high light vary with shade tolerance, but differ between leaf habit groups.