Pre-dawn water potential determines stomatal sensitivity to vapor pressure deficit in trees

Abstract

The balance between terrestrial carbon assimilation and water loss is optimized by stomatal control in leaves. The response of stomatal conductance to increasing vapor pressure deficit (VPD) is critical in the context of climatic change and highly variable between tree species and environments. Why this variability in VPD sensitivity exists is still largely unknown. Yet, as the regulatory cues initiating closure remain unclear, current simulations of forest water use face significant uncertainty. To address this knowledge gap for most of the common European tree species, we present data measured regularly in the crowns of mature trees growing in a natural forest at the Swiss Canopy Crane II (SCCII) site (Basel, Switzerland). We used three years of repeated stomatal conductance measurements across the growing season performed at the leaf level (over 1000 measurements), in combination with concurrent diel leaf water potential measurements and VPD monitoring of over 80 individuals. We show that pre-dawn, rather than the expected midday, tree water status is more critical in adjusting the stomatal closure responses to increasing VPD. A striking reduction can be found in this VPD sensitivity when pre-dawn leaf water potential approaches -1.2 MPa, independent of the species. Only above this threshold, i.e., when trees were well-hydrated, did the species show variance in midday stomatal sensitivity to VPD. This aligns with the commonly adopted hydraulic safety-efficiency theorem for explaining species-specific variance. We argue that daytime canopy conductance does not solely optimize assimilation against the risk of cavitation, which commonly happens during high midday VPD. Rather, our novel finding suggests that mature trees might adjust their water-use strategy to sustain high nighttime turgor pressure (as required for sugar transport and growth), although the regulating mechanisms are yet unknown. The discovery of this uniform pre-dawn threshold across species is particularly critical for reducing uncertainty when modeling forest water use responses to VPD.