& Key message Abundant Neotropical canopy-tree species are more resistant to drought-induced branch embolism than what is currently admitted. Large hydraulic safety margins protect them from hydraulic failure under actual drought conditions. & Context Xylem vulnerability to embolism, which is associated to survival under extreme drought conditions, is being increasingly studied in the tropics, but data on the risk of hydraulic failure for lowland Neotropical rainforest canopy-tree species, thought to be highly vulnerable, are lacking. & Aims The purpose of this study was to gain more knowledge on species drought-resistance characteristics in branches and leaves and the risk of hydraulic failure of abundant rainforest canopy-tree species during the dry season. & Methods We first assessed the range of branch xylem vulnerability to embolism using the flow-centrifuge technique on 1-mlong sun-exposed branches and evaluated hydraulic safety margins with leaf turgor loss point and midday water potential during normal-and severe-intensity dry seasons for a large set of Amazonian rainforest canopy-tree species. & Results Tree species exhibited a broad range of embolism resistance, with the pressure threshold inducing 50% loss of branch hydraulic conductivity varying from − 1.86 to − 7.63 MPa. Conversely, we found low variability in leaf turgor loss point and dry season midday leaf water potential, and mostly large, positive hydraulic safety margins.

Hydraulic segmentation at the stem-leaf transition predicts higher hydraulic resistance in leaves than in stems. Vulnerability segmentation, however, predicts lower embolism resistance in leaves. Both mechanisms should theoretically favour runaway embolism in leaves to preserve expensive organs such as stems, and should be tested for any potential coordination. We investigated the theoretical leaf-specific conductivity based on an anatomical approach to quantify the degree of hydraulic segmentation across 21 tropical rainforest tree species. Xylem resistance to embolism in stems (flow-centrifugation technique) and leaves (optical visualization method) was quantified to assess vulnerability segmentation. We found a pervasive hydraulic segmentation across species, but with a strong variability in the degree of segmentation. Despite a clear continuum in the degree of vulnerability segmentation, eight species showed a positive vulnerability segmentation (leaves less resistant to embolism than stems), whereas the remaining species studied exhibited a negative or no vulnerability segmentation. The degree of vulnerability segmentation was positively related to the degree of hydraulic segmentation, such that segmented species promote both mechanisms to hydraulically decouple leaf xylem from stem xylem. To what extent hydraulic and vulnerability segmentation determine drought resistance requires further integration of the leaf-stem transition at the whole-plant level, including both xylem and outer xylem tissue.

Summary Drought‐induced xylem embolism is considered to be one of the main factors driving mortality in woody plants worldwide. Although several structure–functional mechanisms have been tested to understand the anatomical determinants of embolism resistance, there is a need to study this topic by integrating anatomical data for many species. We combined optical, laser, and transmission electron microscopy to investigate vessel diameter, vessel grouping, and pit membrane ultrastructure for 26 tropical rainforest tree species across three major clades (magnoliids, rosiids, and asteriids). We then related these anatomical observations to previously published data on drought‐induced embolism resistance, with phylogenetic analyses. Vessel diameter, vessel grouping, and pit membrane ultrastructure were all predictive of xylem embolism resistance, but with weak predictive power. While pit membrane thickness was a predictive trait when vestured pits were taken into account, the pit membrane diameter‐to‐thickness ratio suggests a strong importance of the deflection resistance of the pit membrane. However, phylogenetic analyses weakly support adaptive coevolution. Our results emphasize the functional significance of pit membranes for air‐seeding in tropical rainforest trees, highlighting also the need to study their mechanical properties due to the link between embolism resistance and pit membrane diameter‐to‐thickness ratio. Finding support for adaptive coevolution also remains challenging.

Although the leaf economic spectrum has deepened our understanding of leaf trait variability, little is known about how leaf traits scale with leaf area. This uncertainty has resulted in the assumption that leaf traits should vary by keeping the same pace of variation with increases in leaf area across the leaf size range. We evaluated the scaling of morphological, tissue-surface and vascular traits with overall leaf area, and the functional significance of such scaling. We examined 1,271 leaves for morphological traits, and 124 leaves for anatomical and hydraulic traits, from 38 trees of Cecropia obtusa Trécul (Urticaceae) in French Guiana. Cecropia is a Neotropical genus of pioneer trees that can exhibit large laminas (0.4 m2 for C. obtusa), with leaf size ranging by two orders of magnitude. We measured (i) tissue fractions within petioles and their second moment of area, (ii) theoretical xylem hydraulic efficiency of petioles and (iii) the extent of leaf vessel widening within the hydraulic path. We found that different scaling of morphological trait variability allows for optimisation of lamina display among larger leaves, especially the positive allometric relationship between lamina area and petiole cross-sectional area. Increasing the fraction of pith is a key factor that increases the geometrical effect of supportive tissues on mechanical rigidity and thereby increases carbon-use efficiency. We found that increasing xylem hydraulic efficiency with vessel size results in lower leaf lamina area: xylem ratios, which also results in potential carbon savings for large leaves. We found that the vessel widening is consistent with hydraulic optimisation models. Leaf size variability modifies scaling of leaf traits in this large-leaved species.

Embolism spreading in xylem is an important component of plant drought resistance. Since embolism resistance has been shown to be mechanistically linked to pit membrane characters in stem xylem, we speculate that similar mechanisms account for leaf xylem. We conducted transmission electron microscopy to investigate pit membrane characters in leaf xylem across 18 Neotropical tree species. We also conducted gold perfusion and polar lipid detection experiments on three species covering the full range of leaf embolism resistance. We then related these observations to previously published data on embolism resistance of leaf xylem. We also incorporated previously published data on stem embolism resistance and stem xylem pit membranes to investigate the link between vulnerability segmentation (i.e., difference in embolism resistance) and leaf-stem anatomical variation. Pit membrane thickness (Tpm,max) and the pit membrane thickness-to-diameter ratio (Tpm,max/Dpm) were predictive of leaf embolism resistance, especially when vestured pits were taken into account. Variation in Tpm,max/Dpm was the only trait predictive of vulnerability segmentation between leaves and stems. Gold particles of 5 and 10 nm infiltrated pit membranes in three species, while the entry of 50-nm particles was blocked. Moreover, polar lipids were associated with inner conduit walls and pits. Our results suggest that mechanisms related to embolism spreading are determined by pit membrane thickness, pore constrictions (i.e., the narrowest bottlenecks along pore pathways), and lipid surfactants, which are largely similar between leaf and stem xylem and between temperate and tropical trees. However, our mechanistic understanding of embolism propagation and the functional relevance of Tpm,max/Dpm remains elusive.

Climate models predict an increase in the severity and the frequency of droughts. Tropical forests are among the ecosystems that could be highly impacted by these droughts. Here, we explore how hydraulic and photochemical processes respond to drought stress and re-watering. We conducted a pot experiment on saplings of five tree species. Before the onset of drought, we measured a set of hydraulic traits, including minimum leaf conductance, leaf embolism resistance, and turgor loss point. During drought stress, we monitored traits linked to leaf hydraulic functioning (leaf water potential (ψmd) and stomatal conductance (gs)) and traits linked to leaf photochemical functioning (maximum quantum yield of photosystem II (Fv/Fm) and maximum electron transport rate (ETRmax)) at different wilting stages. After re-watering the same traits were measured after 3, 7, and 14 days. Hydraulic trait values decreased faster than photochemical trait values. After re-watering, the values of the four traits recovered at different rates. Fv/Fm recovered very fast close to their initial values only three days after re-watering. This was followed by ETRmax, Ψmd and gs. Finally, we show that species with large stomatal and leaf safety margin and low πtlp are not strongly impacted by drought whereas they have a low recovery on photochemical efficiency. These results demonstrate that πtlp, stomatal and leaf safety margin are a good indicators of plant responses to drought stress and also to recovery for photochemical efficiency.

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.

The leaf size-stem size spectrum is one of the main dimensions of plant ecological strategies. Yet the anatomical, mechanical, and hydraulic implications of small vs. large shoots are still poorly understood. We investigated 42 tropical rainforest tree species in French Guiana, with a wide range of leaf areas at the shoot level. We quantified the scaling of hydraulic and mechanical constraints with shoot size estimated as the water potential difference ΔΨ and the bending angle ΔΦ, respectively. We investigated how anatomical tissue area, flexural stiffness and xylem vascular architecture affect such scaling by deviating (or not) from theoretical isometry with shoot size variation. Vessel diameter and conductive path length were found to be allometrically related to shoot size, thereby explaining the independence between ΔΨ and shoot size. Leaf mass per area, stem length, and the modulus of elasticity were allometrically related with shoot size, explaining the independence between ΔΦ and shoot size. Our study also shows that the maintenance of both water supply and mechanical stability across the shoot size range are not in conflict.