Shoot dimorphism enables Sequoia sempervirens to separate requirements for foliar water uptake and photosynthesis

Abstract

Premise: Trees in wet forests often have features that prevent water films from covering stomata and inhibiting gas exchange, while many trees in drier environments use foliar water uptake to reduce water stress. In forests with both wet and dry seasons, evergreen trees would benefit from producing leaves capable of balancing rainy-season photosynthesis with summertime water absorption. Methods: Using samples collected from across the vertical gradient in tall redwood (Sequoia sempervirens) crowns, we estimated tree-level foliar water uptake and employed physics-based causative modeling to identify key functional traits that determine uptake potential by setting hydraulic resistance. Results: We showed that Sequoia has two functionally distinct shoot morphotypes. While most shoots specialize in photosynthesis, the axial shoot type is capable of much greater foliar water uptake, and its within-crown distribution varies with latitude. A suite of leaf surface traits cause hydraulic resistance, leading to variation in uptake capacity among samples. Conclusions: Shoot dimorphism gives tall Sequoia trees the capacity to absorb up to 48 kg H 2 O h −1 during the first hour of leaf wetting, ameliorating water stress while presumably maintaining high photosynthetic capacity year round. Geographic variation in shoot dimorphism suggests that plasticity in shoot-type distribution and leaf surface traits helps Sequoia maintain a dominate presence in both wet and dry forests.

Towards multivariate functional trait syndromes: Predicting foliar water uptake in trees

“…Differences in the foliar water uptake pathway between angiosperms and conifers may have their roots in the diverging evolutionary ecology of these two clades, in which changes in stomatal function may relate to uptake, photosynthetic rates, and other strategic differences. Stomatal density most likely increases surface hydraulic resistance in conifers because conifers possess large wax plugs in their stomata and their density is associated with a general abundance of epicuticular wax (Chin, Guzmán‐Delgado, Sillett, Orozco, et al, 2022; Chin, Guzmán‐Delgado, Sillett, Kerhoulas, et al, 2022; Leyton & Juniper, 1963; Tianshi & Chau, 2022). Larger guard cells, which are associated with larger stomatal pores, were the individual trait most associated with foliar water uptake in conifers, a trait previously found to reduce surface hydraulic resistance in Sequoia (Chin, Guzmán‐Delgado, Sillett, Orozco, et al, 2022).…”

“…Stomatal density most likely increases surface hydraulic resistance in conifers because conifers possess large wax plugs in their stomata and their density is associated with a general abundance of epicuticular wax (Chin, Guzmán‐Delgado, Sillett, Orozco, et al, 2022; Chin, Guzmán‐Delgado, Sillett, Kerhoulas, et al, 2022; Leyton & Juniper, 1963; Tianshi & Chau, 2022). Larger guard cells, which are associated with larger stomatal pores, were the individual trait most associated with foliar water uptake in conifers, a trait previously found to reduce surface hydraulic resistance in Sequoia (Chin, Guzmán‐Delgado, Sillett, Orozco, et al, 2022). The positive association between uptake and stomatal size implies that some water does enter conifer stomata.…”

“…Trees, and other plants, can absorb water across the surfaces of their leaves when wet or under nearly saturated vapor conditions (Dawson & Goldsmith, 2018; Guzmán‐Delgado et al, 2017; Rundel, 1982; Schreel & Steppe, 2019, 2020). Water is pulled into leaves down the gradient in potential energy (called water potential) that exists between liquid water outside the leaf and the leaf interior, and is slowed by hydraulic resistance imposed by leaf structure (Berry et al, 2019; Chin, Guzmán‐Delgado, Sillett, Orozco, et al, 2022; Guzmán‐Delgado et al, 2018; van den Honert, 1948). Access to above groundwater sources can improve plant water status and carbon balance, repair drought and freeze–thaw‐induced damage such as buckled tracheids and embolisms, extend photosynthetic time, support turgor‐driven cell expansion, as well as provide water to dry soils (Binks et al, 2019; Boanares et al, 2020; Burgess & Dawson, 2004; Chin, Guzmán‐Delgado, Sillett, Kerhoulas, et al, 2022; Eller et al, 2013; Simonin et al, 2009; Steppe et al, 2018).…”

“…In angiosperms, water appears to enter leaves through both stomata and the cuticle (Berry et al, 2019; Binks et al, 2019; Eichert & Goldbach, 2008; Goldsmith et al, 2013; Guzmán‐Delgado et al, 2021; Schreel et al, 2020) and traits such as trichomes can either aid absorption or limit the ability of water to reach the leaf surface (Fernández et al, 2014; Ohrui et al, 2007; Schaepdryver et al, 2022; Schreel et al, 2020). In conifers, less is known, with the cuticle potentially being the primary water absorption point due to wax stomatal plugs, and surface waxiness placing limits on absorption in Sequoia trees (Chin, Guzmán‐Delgado, Sillett, Orozco, et al, 2022; Chin, Guzmán‐Delgado, Sillett, Kerhoulas, et al, 2022). Beyond these surface resistance‐related traits, internal hydraulic resistance may matter.…”

Tracheid buckling buys time, foliar water uptake pays it back: Coordination of leaf structure and function in tall redwood trees

“…Sequoia possesses axial leaves specialized nonphotosynthetic leaf type capable of triple the water absorption rate of the much more abundant peripheral leaves. Axial leaves have more than twice the transfusion tissue area of peripheral leaves and occur only along central woody shoots, likely enhancing their survival and pointing toward a link between transfusion tissue water release capacity and foliar water uptake (Chin et al, 2022). Maximum variability in peripheral‐leaf transfusion tissue investment and peak seconds of ΔE sustained occur in the middle crown at approximately 70 m (Figure 3a,c,e).…”