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.

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.

Contrasting Dependencies of Photosynthetic Capacity on Leaf Nitrogen in Early- and Late-Successional Tropical Montane Tree Species.

Differences in photosynthetic capacity among tree species and tree functional types are currently assumed to be largely driven by variation in leaf nutrient content, particularly nitrogen (N). However, recent studies indicate that leaf N content is often a poor predictor of variation in photosynthetic capacity in tropical trees. In this study, we explored the relative importance of area-based total leaf N content (Ntot) and within-leaf N allocation to photosynthetic capacity versus light-harvesting in controlling the variation in photosynthetic capacity (i.e. V cmax, J max) among mature trees of 12 species belonging to either early (ES) or late successional (LS) groups growing in a tropical montane rainforest in Rwanda, Central Africa. Photosynthetic capacity at a common leaf temperature of 25˚C (i.e. maximum rates of Rubisco carboxylation, V cmax25 and of electron transport, J max25) was higher in ES than in LS species (+ 58% and 68% for V cmax25 and J max25, respectively). While Ntot did not significantly differ between successional groups, the photosynthetic dependency on Ntot was markedly different. In ES species, V cmax25 was strongly and positively related to Ntot but this was not the case in LS species. However, there was no significant trade-off between relative leaf N investments in compounds maximizing photosynthetic capacity versus compounds maximizing light harvesting. Both leaf dark respiration at 25˚C (+ 33%) and, more surprisingly, apparent photosynthetic quantum yield (+ 35%) was higher in ES than in LS species. Moreover, Rd25 was positively related to Ntot for both ES and LS species. Our results imply that efforts to quantify carbon fluxes of tropical montane rainforests would be improved if they considered contrasting within-leaf N allocation and photosynthetic Ntot dependencies between species with different successional strategies.

Traits controlling shade tolerance in tropical montane trees.

Tropical canopies are complex, with multiple canopy layers and pronounced gap dynamics contributing to their high species diversity and productivity. An important reason for this complexity is the large variation in shade tolerance among different tree species. At present, we lack a clear understanding of which plant traits control this variation, e.g., regarding the relative contributions of whole-plant versus leaf traits or structural versus physiological traits. We investigated a broad range of traits in six tropical montane rainforest tree species with different degrees of shade tolerance, grown under three different radiation regimes (under the open sky or beneath sparse or dense canopies). The two distinct shade-tolerant species had higher fractional biomass in leaves and branches while shade-intolerant species invested more into stems, and these differences were greater under low radiation. Leaf respiration and photosynthetic light compensation point did not vary with species shade tolerance, regardless of radiation regime. Leaf temperatures in open plots were markedly higher in shade-tolerant species due to their low transpiration rates and large leaf sizes. Our results suggest that interspecific variation in shade tolerance of tropical montane trees is controlled by species differences in whole-plant biomass allocation strategy rather than by difference in physiological leaf traits determining leaf carbon balance at low radiation.