Lianas in tropical dry seasonal forests have a high hydraulic efficiency but not always a higher embolism resistance than lianas in rainforests.

BACKGROUND AND AIMS: Lianas have higher relative abundance and biomass in drier seasonal forests than rainforests, but whether this difference is associated with their hydraulic strategies is unclear. Here, we investigate whether lianas of seasonally dry forests are safer and more efficient in water transport than rainforest ones, explaining liana abundance patterns. METHODS: We measured hydraulic traits on five pairs of congeneric lianas of the tribe Bignonieae in two contrasting forest sites: the wet 'Dense Ombrophilous Forest' in the Central Amazonia (~ 2 dry months) and the drier 'Semideciduous Seasonal Forest' in the inland Atlantic Forest (~6 dry months). We also gathered a broader database, including 197 trees and 58 liana species from different tropical forests, to compare hydraulic safety between habits and forest types. KEY RESULTS: Bignonieae lianas from both forests had high and similar hydraulic efficiency and exhibited variability in resistance to embolism across forest types when phylogenetic relationships are taken into account. Three genera had higher hydraulic safety in the seasonal forest than in the rainforest, but species across both forests had similar positive hydraulic safety margin despite lower predawn water potential values of seasonal forest' lianas. We did not find the safety-efficiency trade-off. Merging our results with previously published data evidenced a high variability of resistance to embolism in both trees and lianas, independent of forest types. CONCLUSIONS: The high hydraulic efficiency of lianas detected here probably favors their rapid growth across tropical forests, but differences in hydraulic safety highlight that some species are highly vulnerable and may rely on other mechanisms to cope with drought. Future research on the lethal dehydration threshold and the connection between hydraulic resistance strategies and liana abundance could offer further insights into tropical forest dynamics under climatic threats.

Rootstocks affect the vulnerability to embolism and pit membrane thickness in Citrus scions.

Embolism resistance of xylem tissue varies among species and is an important trait related to drought resistance, with anatomical attributes like pit membrane thickness playing an important role in avoiding embolism spread. Grafted Citrus trees are commonly grown in orchards, with the rootstock being able to affect the drought resistance of the whole plant. Here, we evaluated how rootstocks affect the vulnerability to embolism resistance of the scion using several rootstock/scion combinations. Scions of 'Tahiti' acid lime, 'Hamlin', 'Pera' and 'Valencia' oranges grafted on a 'Rangpur' lime rootstock exhibit similar vulnerability to embolism. In field-grown trees, measurements of leaf water potential did not suggest significant embolism formation during the dry season, while stomata of Citrus trees presented an isohydric response to declining water availability. When 'Valencia' orange scions were grafted on 'Rangpur' lime, 'IAC 1710' citrandarin, 'Sunki Tropical' mandarin or 'Swingle' citrumelo rootstocks, variation in intervessel pit membrane thickness of the scion was found. The 'Rangpur' lime rootstock, which is known for its drought resistance, induced thicker pit membranes in the scion, resulting in higher embolism resistance than the other rootstocks. Similarly, the rootstock 'IAC 1710' citrandarin generated increased embolism resistance of the scion, which is highly relevant for citriculture.

Lipid concentration and composition in xylem sap of woody angiosperms from a tropical savanna and a seasonal rainforest.

Lipids may play an important role in preventing gas embolisms by coating nanobubbles in xylem sap. Few studies on xylem sap lipids have been reported for temperate plants, and it remain unclear whether sap lipids have adaptational significance in tropical plants. In this study, we quantify the lipid composition of xylem sap for angiosperm species from a tropical savanna (seven species) and a seasonal rainforest (five species) using mass spectrometry. We found that all twelve species studied contained lipids in their xylem sap, including galactolipids, phospholipids and triacylglycerol, with a total lipid concentration ranging from 0.09 to 0.26 nmol/L. There was no difference in lipid concentration or composition between plants from the two sites, and the lipid concentration was negatively related to species' open vessel volume. Furthermore, savanna species showed little variation in lipid composition between the dry and the rainy season. These results support the hypothesis that xylem sap lipids are derived from the cytoplasm of individual conduit cells, remain trapped inside individual conduits, and undergo few changes in composition over consecutive seasons. A xylem sap lipidomic data set, which includes 12 tropical tree species from this study and 11 temperate tree species from literature, revealed no phylogenetic signals in lipid composition for these species. This study fills a knowledge gap in the lipid content of xylem sap in tropical trees and provides additional support for their common distribution in xylem sap of woody angiosperms. It appears that xylem sap lipids have no adaptive significance.

Gold perfusion experiments support the multi-layered, mesoporous nature of intervessel pit membranes in angiosperm xylem.

Fluid transport across intervessel pit membranes of angiosperm xylem plays a major role in plant transpiration, with transport resistance largely depending on pore constriction sizes. Traditionally, fluid particles traversing pit membranes are assumed to cross a single instead of multiple pore constrictions. We tested a multi-layered pit membrane model in xylem of eight angiosperm species by estimating the size frequency of pore constrictions in relation to pit membrane thickness and compared modelled data with perfusion characteristics of nanoscale gold particles based on transmission electron microscopy. The size frequency of modelled pore constrictions showed similar patterns to the measured number of perfused particle sizes inside pit membranes, although frequency values measured were 10-50 times below modelled data. Small particles enter pit membranes most easily, especially when injected in thin pit membranes. The trapping of gold particles by pore constrictions becomes more likely with increasing pore constriction number and pit membrane thickness. While quantitative differences between modelled and experimental data are due to various practical limitations, their qualitative agreement supports a multi-layered pit membrane model with multiple pore constrictions. Pore constrictions between 5 and 50 nm are realistic, and confirm the mesoporous nature of pit membranes.

Hydraulic variability of tropical forests is largely independent of water availability.

Tropical rainforest woody plants have been thought to have uniformly low resistance to hydraulic failure and to function near the edge of their hydraulic safety margin (HSM), making these ecosystems vulnerable to drought; however, this may not be the case. Using data collected at 30 tropical forest sites for three key traits associated with drought tolerance, we show that site-level hydraulic diversity of leaf turgor loss point, resistance to embolism (P50 ), and HSMs is high across tropical forests and largely independent of water availability. Species with high HSMs (>1 MPa) and low P50 values (< -2 MPa) are common across the wet and dry tropics. This high site-level hydraulic diversity, largely decoupled from water stress, could influence which species are favoured and become dominant under a drying climate. High hydraulic diversity could also make these ecosystems more resilient to variable rainfall regimes.

Rooting depth and xylem vulnerability are independent woody plant traits jointly selected by aridity, seasonality, and water table depth.

Evolutionary radiations of woody taxa within arid environments were made possible by multiple trait innovations including deep roots and embolism-resistant xylem, but little is known about how these traits have coevolved across the phylogeny of woody plants or how they jointly influence the distribution of species. We synthesized global trait and vegetation plot datasets to examine how rooting depth and xylem vulnerability across 188 woody plant species interact with aridity, precipitation seasonality, and water table depth to influence species occurrence probabilities across all biomes. Xylem resistance to embolism and rooting depth are independent woody plant traits that do not exhibit an interspecific trade-off. Resistant xylem and deep roots increase occurrence probabilities in arid, seasonal climates over deep water tables. Resistant xylem and shallow roots increase occurrence probabilities in arid, nonseasonal climates over deep water tables. Vulnerable xylem and deep roots increase occurrence probabilities in arid, nonseasonal climates over shallow water tables. Lastly, vulnerable xylem and shallow roots increase occurrence probabilities in humid climates. Each combination of trait values optimizes occurrence probabilities in unique environmental conditions. Responses of deeply rooted vegetation may be buffered if evaporative demand changes faster than water table depth under climate change.

Hydraulic traits and photosynthesis are coordinated with trunk sapwood capacitance in tropical tree species.

Water stored in trunk sapwood is vital for the canopy to maintain its physiological function under high transpiration demands. Little is known regarding the anatomical properties that contribute to the hydraulic capacitance of tree trunks and whether trunk capacitance is correlated with the hydraulic and gas exchange traits of canopy branches. We examined sapwood capacitance, xylem anatomical characteristics of tree trunks, embolism resistance, the minimal xylem water potential of canopy branches, leaf photosynthesis and stomatal conductance in 22 species from a tropical seasonal rainforest and savanna. The results showed that the mean trunk sapwood capacitance did not differ between the two biomes. Capacitance was closely related to the fiber lumen fraction and fiber wall reinforcement and not to the axial and ray parenchyma fractions. Additionally, it was positively correlated with the theoretical hydraulic conductivity of a trunk and the specific hydraulic conductivity of branches, and showed a trade-off with branch embolism resistance. Species with a high trunk sapwood capacitance maintained less negative canopy water potentials in the dry season, but higher leaf photosynthetic rates and stomatal conductance in the wet season. This study provides a functional link among trunk sapwood capacitance, xylem anatomy, canopy hydraulics and photosynthesis in tropical trees.

Angiosperms follow a convex trade-off to optimize hydraulic safety and efficiency.

Intervessel pits are considered to function as valves that avoid embolism spreading and optimize efficient transport of xylem sap across neighbouring vessels. Hydraulic transport between vessels would therefore follow a safety-efficiency trade-off, which is directly related to the total intervessel pit area (Ap ), inversely related to the pit membrane thickness (TPM ) and driven by a pressure difference. To test this hypothesis, we modelled the relative transport rate of gas (ka ) and water (Q) at the intervessel pit level for 23 angiosperm species and correlated these parameters with the water potential at which 50% of embolism occurs (Ψ50 ). We also measured ka for 10 species using pneumatic measurements. The pressure difference across adjacent vessels and estimated values of ka and Q were related to Ψ50 , following a convex safety-efficiency trade-off based on modelled and experimental data. Minor changes in TPM and Ap exponentially affected the pressure difference and flow, respectively. Our results provide clear evidence that a xylem safety-efficiency trade-off is not linear, but convex due to flow across intervessel pit membranes, which represent mesoporous media within microporous conduits. Moreover, the convex nature of long-distance xylem transport may contribute to an adjustable fluid balance of plants, depending on environmental conditions.

Lipid-Coated Nanobubbles in Plants.

One of the more surprising occurrences of bulk nanobubbles is in the sap inside the vascular transport system of flowering plants, the xylem. In plants, nanobubbles are subjected to negative pressure in the water and to large pressure fluctuations, sometimes encompassing pressure changes of several MPa over the course of a single day, as well as wide temperature fluctuations. Here, we review the evidence for nanobubbles in plants and for polar lipids that coat them, allowing nanobubbles to persist in this dynamic environment. The review addresses how the dynamic surface tension of polar lipid monolayers allows nanobubbles to avoid dissolution or unstable expansion under negative liquid pressure. In addition, we discuss theoretical considerations about the formation of lipid-coated nanobubbles in plants from gas-filled spaces in the xylem and the role of mesoporous fibrous pit membranes between xylem conduits in creating the bubbles, driven by the pressure gradient between the gas and liquid phase. We discuss the role of surface charges in preventing nanobubble coalescence, and conclude by addressing a number of open questions about nanobubbles in plants.

Optimal balancing of xylem efficiency and safety explains plant vulnerability to drought.

In vast areas of the world, forests and vegetation are water limited and plant survival depends on the ability to avoid catastrophic hydraulic failure. Therefore, it is remarkable that plants take hydraulic risks by operating at water potentials (ψ) that induce partial failure of the water conduits (xylem). Here we present an eco-evolutionary optimality principle for xylem conduit design that explains this phenomenon based on the hypothesis that conductive efficiency and safety are optimally co-adapted to the environment. The model explains the relationship between the tolerance to negative water potential (ψ50 ) and the environmentally dependent minimum ψ (ψmin ) across a large number of species, and along the xylem pathway within individuals of two species studied. The wider hydraulic safety margin in gymnosperms compared to angiosperms can be explained as an adaptation to a higher susceptibility to accumulation of embolism. The model provides a novel optimality-based perspective on the relationship between xylem safety and efficiency.

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.

Global beta-diversity of angiosperm trees is shaped by Quaternary climate change.

As Earth's climate has varied strongly through geological time, studying the impacts of past climate change on biodiversity helps to understand the risks from future climate change. However, it remains unclear how paleoclimate shapes spatial variation in biodiversity. Here, we assessed the influence of Quaternary climate change on spatial dissimilarity in taxonomic, phylogenetic, and functional composition among neighboring 200-kilometer cells (beta-diversity) for angiosperm trees worldwide. We found that larger glacial-interglacial temperature change was strongly associated with lower spatial turnover (species replacements) and higher nestedness (richness changes) components of beta-diversity across all three biodiversity facets. Moreover, phylogenetic and functional turnover was lower and nestedness higher than random expectations based on taxonomic beta-diversity in regions that experienced large temperature change, reflecting phylogenetically and functionally selective processes in species replacement, extinction, and colonization during glacial-interglacial oscillations. Our results suggest that future human-driven climate change could cause local homogenization and reduction in taxonomic, phylogenetic, and functional diversity of angiosperm trees worldwide.

Ageing-induced shrinkage of intervessel pit membranes in xylem of Clematis vitalba modifies its mechanical properties as revealed by atomic force microscopy.

Bordered pit membranes of angiosperm xylem are anisotropic, mesoporous media between neighbouring conduits, with a key role in long distance water transport. Yet, their mechanical properties are poorly understood. Here, we aim to quantify the stiffness of intervessel pit membranes over various growing seasons. By applying an AFM-based indentation technique "Quantitative Imaging" we measured the effective elastic modulus (E effective) of intervessel pit membranes of Clematis vitalba in dependence of size, age, and hydration state. The indentation-deformation behaviour was analysed with a non-linear membrane model, and paired with magnetic resonance imaging to visualise sap-filled and embolised vessels, while geometrical data of bordered pits were obtained using electron microscopy. E effective was transformed to the geometrically independent apparent elastic modulus E apparent and to aspiration pressure P b. The material stiffness (E apparent) of fresh pit membranes was with 57 MPa considerably lower than previously suggested. The estimated pressure for pit membrane aspiration was 2.20+28 MPa. Pit membranes from older growth rings were shrunken, had a higher material stiffness and a lower aspiration pressure than current year ones, suggesting an irreversible, mechanical ageing process. This study provides an experimental-stiffness analysis of hydrated intervessel pit membranes in their native state. The estimated aspiration pressure suggests that membranes are not deflected under normal field conditions. Although absolute values should be interpreted carefully, our data suggest that pit membrane shrinkage implies increasing material stiffness, and highlight the dynamic changes of pit membrane mechanics and their complex, functional behaviour for fluid transport.

Addressing controversies in the xylem embolism resistance-vessel diameter relationship.

Although xylem embolism is a key process during drought-induced tree mortality, its relationship to wood anatomy remains debated. While the functional link between bordered pits and embolism resistance is known, there is no direct, mechanistic explanation for the traditional assumption that wider vessels are more vulnerable than narrow ones. We used data from 20 temperate broad-leaved tree species to study the inter- and intraspecific relationship of water potential at 50% loss of conductivity (P50 ) with hydraulically weighted vessel diameter (Dh ) and tested its link to pit membrane thickness (TPM ) and specific conductivity (Ks ) on species level. Embolism-resistant species had thick pit membranes and narrow vessels. While Dh was weakly associated with TPM , the P50 -Dh relationship remained highly significant after accounting for TPM . The interspecific pattern between P50 and Dh was mirrored by a link between P50 and Ks , but there was no evidence for an intraspecific relationship. Our results provide robust evidence for an interspecific P50 -Dh relationship across our species. As a potential cause for the inconsistencies in published P50 -Dh relationships, our analysis suggests differences in the range of trait values covered, and the level of data aggregation (species, tree or sample level) studied.

Plant hydraulic modelling of leaf and canopy fuel moisture content reveals increasing vulnerability of a Mediterranean forest to wildfires under extreme drought.

Fuel moisture content (FMC) is a crucial driver of forest fires in many regions world-wide. Yet, the dynamics of FMC in forest canopies as well as their physiological and environmental determinants remain poorly understood, especially under extreme drought. We embedded a FMC module in the trait-based, plant-hydraulic SurEau-Ecos model to provide innovative process-based predictions of leaf live fuel moisture content (LFMC) and canopy fuel moisture content (CFMC) based on leaf water potential ( ψ Leaf ). SurEau-Ecos-FMC relies on pressure-volume (p-v) curves to simulate LFMC and vulnerability curves to cavitation to simulate foliage mortality. SurEau-Ecos-FMC accurately reproduced ψ Leaf and LFMC dynamics as well as the occurrence of foliage mortality in a Mediterranean Quercus ilex forest. Several traits related to water use (leaf area index, available soil water, and transpiration regulation), vulnerability to cavitation, and p-v curves (full turgor osmotic potential) had the greatest influence on LFMC and CFMC dynamics. As the climate gets drier, our results showed that drought-induced foliage mortality is expected to increase, thereby significantly decreasing CFMC. Our results represent an important advance in our capacity to understand and predict the sensitivity of forests to wildfires.

A reduced role for water transport during the Cenozoic evolution of epiphytic Eupolypod ferns.

The Cretaceous-Cenozoic expansion of tropical forests created canopy space that was subsequently occupied by diverse epiphytic communities including Eupolypod ferns. Eupolypods proliferated in this more stressful niche, where lower competition enabled the adaptive radiation of thousands of species. Here, we examine whether xylem traits helped shape the Cenozoic radiation of Eupolypod ferns. We characterized the petiole xylem anatomy of 39 species belonging to the Eupolypod I and Eupolypod II clades occupying the epiphytic, hemiepiphytic, and terrestrial niche, and we assessed vulnerability to embolism in a subset of species. The transition to the canopy was associated with reduced xylem content and smaller tracheid diameters, but no differences were found in species vulnerability to embolism and pit membrane thickness. Phylogenetic analyses support selection for traits associated with reduced water transport in Eupolypod 1 species. We posit that in Eupolypod epiphytes, selection favored water retention via thicker leaves and lower stomatal density over higher rates of water transport. Consequently, lower leaf water loss was coupled with smaller quantities of xylem and narrower tracheid diameters. Traits associated with water conservation were evident in terrestrial Eupolypod 1 ferns and may have predisposed this clade toward radiation in the canopy.

The relative area of vessels in xylem correlates with stem embolism resistance within and between genera.

The resistance of xylem conduits to embolism is a major factor defining drought tolerance and can set the distributional limits of species across rainfall gradients. Recent work suggests that the proximity of vessels to neighbors increases the vulnerability of a conduit. We therefore investigated whether the relative vessel area of xylem correlates with intra- and inter-generic variation in xylem embolism resistance in species pairs or triplets from the genera Acer, Cinnamomum, Ilex, Quercus and Persea, adapted to environments differing in aridity. We used the optical vulnerability method to assess embolism resistance in stems and conducted anatomical measurements on the xylem in which embolism resistance was quantified. Vessel lumen fraction (VLF) correlated with xylem embolism resistance across and within genera. A low VLF likely increases the resistance to gas movement between conduits, by diffusion or advection, whereas a high VLF enhances gas transport thorough increased conduit-to-conduit connectivity and reduced distances between conduits and therefore the likelihood of embolism propagation. We suggest that the rate of gas movement due to local pressure differences and xylem network connectivity is a central driver of embolism propagation in angiosperm vessels.

A unit pipe pneumatic model to simulate gas kinetics during measurements of embolism in excised angiosperm xylem.

The pneumatic method has been introduced to quantify embolism resistance in plant xylem of various organs by applying a partial vacuum to cut-open xylem. Despite the similarity in vulnerability curves between the pneumatic and other methods, a modeling approach is needed to investigate if changes in xylem embolism during dehydration can be accurately quantified based on gas diffusion kinetics. Therefore, a unit pipe pneumatic (UPPn) model was developed to estimate gas extraction from intact conduits, which were axially interconnected by inter-conduit pit membranes to cut-open conduits. The physical laws used included Fick's law for diffusion, Henry's law for gas concentration partitioning between liquid and gas phases at equilibrium and the ideal gas law. The UPPn model showed that 91% of the extracted gas came from the first five series of embolized, intact conduits and only 9% from the aqueous phase after 15 s of simulation. Considering alternative gas sources, embolism resistance measured with a pneumatron device was systematically overestimated by 2-17%, which corresponded to a typical measuring error of 0.11 MPa for P50 (the water potential equivalent to 50% of the maximum amount of gas extracted). It is concluded that pneumatic vulnerability curves directly measure embolism of intact conduits due to the fast movement of gas across interconduit pit membranes, while gas extraction from sap and diffusion across hydrated cell walls is about 100 times slower. We expect that the UPPn model will also contribute to the understanding of embolism propagation based on temporal gas dynamics.

Functional xylem characteristics associated with drought-induced embolism in angiosperms.

Hydraulic failure resulting from drought-induced embolism in the xylem of plants is a key determinant of reduced productivity and mortality. Methods to assess this vulnerability are difficult to achieve at scale, leading to alternative metrics and correlations with more easily measured traits. These efforts have led to the longstanding and pervasive assumed mechanistic link between vessel diameter and vulnerability in angiosperms. However, there are at least two problems with this assumption that requires critical re-evaluation: (1) our current understanding of drought-induced embolism does not provide a mechanistic explanation why increased vessel width should lead to greater vulnerability, and (2) the most recent advancements in nanoscale embolism processes suggest that vessel diameter is not a direct driver. Here, we review data from physiological and comparative wood anatomy studies, highlighting the potential anatomical and physicochemical drivers of embolism formation and spread. We then put forward key knowledge gaps, emphasising what is known, unknown and speculation. A meaningful evaluation of the diameter-vulnerability link will require a better mechanistic understanding of the biophysical processes at the nanoscale level that determine embolism formation and spread, which will in turn lead to more accurate predictions of how water transport in plants is affected by drought.