Optimal stomatal drought response shaped by competition for water and hydraulic risk can explain plant trait covariation

Abstract

Summary 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.

Climate and functional traits jointly mediate tree water‐use strategies

“…All the studied water-relations traits (except Ψ TLP ) were related to β VPD , whereby the species with more 'efficient' water transport or less 'safe' traits showed higher β VPD . These results are consistent with previous studies relating stomatal responses and water relation traits (Lu et al, 2020) and with the stomatal gas exchange optimization theory (see Tyree & Sperry, 1988;Wang et al, 2020). By contrast, after controlling for climate and tree height, conductance sensitivity to SWC (β SWC ) was only (negatively) related to L s .…”

Effects of Increased N Deposition on Leaf Functional Traits of Four Contrasting Tree Species in Northeast China

“…Correlations were more consistent in gymnosperms, likely because evergreens such as P. koraiensis often hold more mechanical tissues which could help avoiding damage as result of frost or drought [ 59 ]. In previous studies LD of woody species was furthermore found negatively related to the fractions of epidermis and mesophyll but positively related to the fraction of sclerified tissues [ 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 ]. In partial contrast to our second hypothesis we did not find correlations of LD (and LT) with epidermis and mesophyll thicknesses in the studied gymnosperms; variable cell sizes and number [ 19 , 60 ] and air spaces may thus explain differences in LD (and LT) beside changes in structural tissue fractions [ 14 , 46 ].…”

“…However, while effects of N availability on leaf morphological traits have received considerable attention, studies including accompanying changes of leaf anatomical traits are rare [ 27 ]. This is surprising, as changes in, e.g., the size and density of stomata, veins and mesophyll tissue structure affect the performance of photosynthesis and transpiration [ 28 , 29 , 30 , 31 ]. As leaves are contributing 30–80% of the whole-plant hydraulic resistance, hydraulic traits have in particular the potential to affect photosynthetic performance—independent of LMA variation [ 31 ].…”

Parsimony vs predictive and functional performance of three stomatal optimization principles in a big‐leaf framework

“…Ó 2021 The Authors New Phytologist Ó 2021 New Phytologist Foundation New Phytologist (2021) 231: 586-600 www.newphytologist.com carbon maximization. The higher functional accuracy of WUE may indicate that the associated ∂Θ=∂T functional form represents some longer-term ecosystem optimization reflected in observations (Lu et al, 2020), which are not captured by CM and SOX. As such, stomatal optimization based on xylem vulnerability had limited utility in improving modeled interactions between θ, D, and LE at ecosystem scales.…”