Residual water losses mediate the trade-off between growth and drought-survival across saplings of 12 tropical rainforest tree species with contrasting hydraulic strategies.

Knowledge of the physiological mechanisms underlying species vulnerability to drought is critical to better understand patterns of tree mortality. Investigating plant adaptive strategies to drought should thus help to fill this knowledge gap, especially in tropical rainforests exhibiting high functional diversity. In a semi-controlled drought experiment on 12 rainforest tree species, we investigated the diversity in hydraulic strategies and whether they determined the ability of saplings to use stored non-structural carbohydrates during an extreme imposed drought. We further explored the importance of water- and carbon-use strategies in relation to drought-survival through a modelling approach. Hydraulic strategies varied considerably across species with a continuum between dehydration- tolerance and -avoidance. During dehydration leading to hydraulic failure and irrespective of hydraulic strategies, species showed strong declines in whole-plant starch concentrations and a maintenance or even an increase in soluble sugar concentrations potentially favouring osmotic adjustments. Residual water losses mediated the trade-off between time to hydraulic failure and growth, suggesting that it is linked to the 'fast-slow' continuum of plant performances and that dehydration avoidance is an effective drought-survival strategy at the sapling stage. Further investigations on residual water losses may be key to understanding the response of tropical rainforest tree communities to climate change.

Thresholds for persistent leaf photochemical damage predict plant drought resilience in a tropical rainforest.

Water stress can cause declines in plant function that persist after rehydration. Recent work has defined 'resilience' traits characterizing leaf resistance to persistent damage from drought, but whether these traits predict resilience in whole-plant function is unknown. It is also unknown whether the coordination between resilience and 'resistance' - the ability to maintain function during drought - observed globally occurs within ecosystems. For eight rainforest species, we dehydrated and subsequently rehydrated leaves, and measured water stress thresholds for declines in rehydration capacity and maximum quantum yield of photosystem II (Fv /Fm ). We tested correlations with embolism resistance and dry season water potentials (ΨMD ), and calculated safety margins for damage (ΨMD - thresholds) and tested correlations with drought resilience in sap flow and growth. Ψ thresholds for persistent declines in Fv /Fm , indicating resilience, were positively correlated with ΨMD and thresholds for leaf vein embolism. Safety margins for persistent declines in Fv /Fm , but not rehydration capacity, were positively correlated with drought resilience in sap flow. Correlations between resistance and resilience suggest that species' differences in performance during drought are perpetuated after drought, potentially accelerating shifts in forest composition. Resilience to photochemical damage emerged as a promising functional trait to characterize whole-plant drought resilience.

Pit characters determine drought-induced embolism resistance of leaf xylem across 18 Neotropical tree 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. Maximum 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 Tpm, 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.

Modeling the Impact of Proportion, Sowing Date, and Architectural Traits of a Companion Crop on Foliar Fungal Pathogens of Wheat in Crop Mixtures.

Diversification of cropping systems is a lever for the management of epidemics. However, most research to date has focused on cultivar mixtures, especially for cereals, even though crop mixtures can also improve disease management. To investigate the benefits of crop mixtures, we studied the effect of different crop mixture characteristics (i.e., companion proportion, sowing date, and traits) on the protective effect of the mixture. We developed a SEIR (Susceptible, Exposed, Infectious, Removed) model of two damaging wheat diseases (Zymoseptoria tritici and Puccinia triticina), which were applied to different canopy components, ascribable to wheat and a theoretical companion crop. We used the model to study the sensitivity of disease intensity to the following parameters: wheat-versus-companion proportion, companion sowing date and growth, and architectural traits. For both pathogens, the companion proportion had the strongest effect, with 25% of companion reducing disease severity by 50%. However, changing companion growth and architectural traits also significantly improved the protective effect. The effect of companion characteristics was consistent across different weather conditions. After decomposing the dilution and barrier effects, the model suggested that the barrier effect is maximized for an intermediate proportion of companion crop. Our study thus supports crop mixtures as a promising strategy to improve disease management. Future studies should identify real species and determine the combination of host and companion traits to maximize the protective effect of the mixture. [Formula: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Linking drought-induced xylem embolism resistance to wood anatomical traits in Neotropical trees.

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.

Anatomies, vascular architectures, and mechanics underlying the leaf size-stem size spectrum in 42 Neotropical tree species.

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 versus 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 to 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.

Vulnerability and hydraulic segmentations at the stem-leaf transition: coordination across Neotropical trees.

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.

Drought stress recovery of hydraulic and photochemical processes in Neotropical tree saplings.

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 3 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.

Scaling of petiole anatomies, mechanics and vasculatures with leaf size in the widespread Neotropical pioneer tree species Cecropia obtusa Trécul (Urticaceae).

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.