Is vulnerability segmentation at the leaf-stem transition a drought resistance mechanism? A theoretical test with a trait-based model for Neotropical canopy tree species

Abstract

Key message Leaf-stem vulnerability segmentation predicts lower xylem embolism resistance in leaves than stem. However, although it has been intensively investigated these past decades, the extent to which vulnerability segmentation promotes drought resistance is not well understood. Based on a trait-based model, this study theoretically supports that vulnerability segmentation enhances shoot desiccation time across 18 Neotropical tree species. Context Leaf-stem vulnerability segmentation predicts lower xylem embolism resistance in leaves than stems thereby preserving expensive organs such as branches or the trunk. Although vulnerability segmentation has been intensively investigated these past decades to test its consistency across species, the extent to which vulnerability segmentation promotes drought resistance is not well understood. Aims We investigated the theoretical impact of the degree of vulnerability segmentation on shoot desiccation time estimated with a simple trait-based model. Methods We combined data from 18 tropical rainforest canopy tree species on embolism resistance of stem xylem (flow-centrifugation technique) and leaves (optical visualisation method). Measured water loss under minimum leaf and bark conductance, leaf and stem capacitance, and leaf-to-bark area ratio allowed us to calculate a theoretical shoot desiccation time (tcrit). Results Large degrees of vulnerability segmentation strongly enhanced the theoretical shoot desiccation time, suggesting vulnerability segmentation to be an efficient drought resistance mechanism for half of the studied species. The difference between leaf and bark area, rather than the minimum leaf and bark conductance, determined the drastic reduction of total transpiration by segmentation during severe drought. Conclusion Our study strongly suggests that vulnerability segmentation is an important drought resistance mechanism that should be better taken into account when investigating plant drought resistance and modelling vegetation. We discuss future directions for improving model assumptions with empirical measures, such as changes in total shoot transpiration after leaf xylem embolism.

Large leaf hydraulic safety margins limit the risk of drought‐induced leaf hydraulic dysfunction in Neotropical rainforest canopy tree species

“…At our site, coexisting tree species exhibited broad variation in leaf and stem stomatal safety margins (this study; Ziegler et al, 2019), vulnerability segmentation (Levionnois et al, 2020) and residual leaf and bark conductance (Levionnois et al, 2021). The coordination among these traits may influence the likelihood of tree hydraulic damage and mortality risk with the increased occurrence of extreme drought events (Brodribb et al, 2020).…”

“…Therefore, the water potential causing a 50% loss in leaf xylem conductance (P 50,leaf ; MPa) is a crucial threshold, especially for species showing leaf‐stem vulnerability segmentation, with leaves being more vulnerable to the loss of conductance than stems (P 50,leaf > P 50,stem ). Indeed, the magnitudes of the leaf hydraulic safety margin (P min − P 50,leaf ; HSM leaf ) and of the leaf stomatal safety margin (P tlp − P 50,leaf ; SSM leaf ) partly determine the timing of the loss in leaf xylem hydraulic conductance, and consequently influence whole‐plant desiccation time (Blackman, Li, et al, 2019; Levionnois et al, 2021). Drastic losses of leaf xylem conductance may strongly impact tree assimilation and productivity (Brodribb et al, 2021; Scoffoni et al, 2016), which is detrimental since re‐growing stem xylem is an important post‐drought recovery mechanism (Brodribb et al, 2021; Creek et al, 2018; Gauthey et al, 2022).…”

“…Stomatal closure is known to precede and delay embolism formation in stem xylem (Martin‐StPaul et al, 2017; Mencuccini et al, 2015). Additionally, leaf‐stem vulnerability segmentation, when leaf xylem is more vulnerable to drought‐induced embolism than stem xylem, has been reported for some species (Hochberg et al, 2016; Klepsch et al, 2018; Levionnois et al, 2020; Li et al, 2020; Rodriguez‐Dominguez et al, 2018; Skelton et al, 2017; Skelton et al, 2018; Smith‐Martin et al, 2020) and has been suggested as a mechanisms that slows down plant desiccation, since leaf xylem embolism allows a drastic reduction of leaf evaporative surface area (Blackman, Li, et al, 2019; Levionnois et al, 2021).…”

Climate anomalies and neighbourhood crowding interact in shaping tree growth in old‐growth and selectively logged tropical forests

“…We combined our measurements for the six leaf traits with data from previous field campaigns conducted at Paracou (Levionnois et al, 2021;Maréchaux et al, 2015Maréchaux et al, , 2019Ziegler et al, 2019). We further compiled trait data for the 102 focal tree species for six leaf and wood traits that relate to light capture and carbon use from previous work conducted in French Guiana (Baraloto et al, 2010;Fortunel et al, 2012;Vleminckx et al, 2021).…”

Exploring within‐plant hydraulic trait variation: A test of the vulnerability segmentation hypothesis

“…This suggests environmental forcing alone is unlikely to explain segmentation differences. In the few studies examining how vulnerability segmentation impacts plant function and drought resistance, neither reverse segmentation nor interactions with other traits (including hydraulic segmentation and safety [$${P}_{50}$$]) were explored (Blackman et al, 2019; Levionnois et al, 2021; Sperry & Love, 2015).…”