Leaf and twig traits predict habitat adaptation and demographic strategies in tropical freshwater swamp forest trees.

Differences in demographic and environmental niches facilitate plant species coexistence in tropical forests. However, the adaptations that enable species to achieve higher demographic rates (e.g. growth or survival) or occupy unique environmental niches (e.g. waterlogged conditions) remain poorly understood. Anatomical traits may better predict plant environmental and demographic strategies because they are direct measurements of structures involved in these adaptations. We collected 18 leaf and twig traits from 29 tree species in a tropical freshwater swamp forest in Singapore. We estimated demographic parameters of the 29 species from growth and survival models, and degree of association toward swamp habitats. We examined pairwise trait-trait, trait-demography and trait-environment links while controlling for phylogeny. Leaf and twig anatomical traits were better predictors of all demographic parameters than other commonly measured leaf and wood traits. Plants with wider vessels had faster growth rates but lower survival rates. Leaf and spongy mesophyll thickness predicted swamp association. These findings demonstrate the utility of anatomical traits as indicators of plant hydraulic strategies and their links to growth-mortality trade-offs and waterlogging stress tolerance that underlie species coexistence mechanisms in tropical forest trees.

Effects of lianas on forest biogeochemistry during their lives and afterlives.

Climate change and other anthropogenic disturbances are increasing liana abundance and biomass in many tropical and subtropical forests. While the effects of living lianas on species diversity, ecosystem carbon, and nutrient dynamics are receiving increasing attention, the role of dead lianas in forest ecosystems has been little studied and is poorly understood. Trees and lianas coexist as the major woody components of forests worldwide, but they have very different ecological strategies, with lianas relying on trees for mechanical support. Consequently, trees and lianas have evolved highly divergent stem, leaf, and root traits. Here we show that this trait divergence is likely to persist after death, into the afterlives of these organs, leading to divergent effects on forest biogeochemistry. We introduce a conceptual framework combining horizontal, vertical, and time dimensions for the effects of liana proliferation and liana tissue decomposition on ecosystem carbon and nutrient cycling. We propose a series of empirical studies comparing traits between lianas and trees to answer questions concerning the influence of trait afterlives on the decomposability of liana and tree organs. Such studies will increase our understanding of the contribution of lianas to terrestrial biogeochemical cycling, and help predict the effects of their increasing abundance.

Hydraulic vulnerability segmentation in compound-leaved trees: Evidence from an embolism visualization technique.

The hydraulic vulnerability segmentation (HVS) hypothesis implies the existence of differences in embolism resistance between plant organs along the xylem pathway and has been suggested as an adaptation allowing the differential preservation of more resource-rich tissues during drought stress. Compound leaves in trees are considered a low-cost means of increasing leaf area and may thus be expected to show evidence of strong HVS, given the tendency of compound-leaved tree species to shed their leaf units during drought. However, the existence and role of HVS in compound-leaved tree species during drought remain uncertain. We used an optical visualization technique to estimate embolism occurrence in stems, petioles, and leaflets of shoots in two compound-leaved tree species, Manchurian ash (Fraxinus mandshurica) and Manchurian walnut (Juglans mandshurica). We found higher (less negative) water potentials corresponding to 50% loss of conductivity (P50) in leaflets and petioles than in stems in both species. Overall, we observed a consistent pattern of stem > petiole > leaflet in terms of xylem resistance to embolism and hydraulic safety margins (i.e. the difference between mid-day water potential and P50). The coordinated variation in embolism vulnerability between organs suggests that during drought conditions, trees benefit from early embolism and subsequent shedding of more expendable organs such as leaflets and petioles, as this provides a degree of protection to the integrity of the hydraulic system of the more carbon costly stems. Our results highlight the importance of HVS as an adaptive mechanism of compound-leaved trees to withstand drought stress.

Divergent leaf and fine root "pressure-volume relationships" across habitats with varying water availability.

Fine roots and leaves, the direct interfaces of plants with their external environment along the soil-plant-atmosphere continuum, are at the front line to ensure plant adaptation to their growing habitat. This study aimed to compare the vulnerability to water deficit of fine roots and leaves of woody species from karst and mangrove forests-two water-stressed habitats-against that of timber and ornamental woody species grown in a well-watered common garden. Thus, pressure-volume curves in both organs of 37 species (about 12 species from each habitat) were constructed. Fine roots wilted at a less negative water potential than leaves in 32 species and before branch xylem lost 50% of its hydraulic conductivity in the 17 species with available data on branch xylem embolism resistance. Thus, turgor loss in fine roots can act as a hydraulic fuse mechanism against water stress. Mangroves had higher leaf resistance against wilting and lower leaf-specific area than the karst and common garden plants. Their fine roots had high specific root lengths (SRL) and high capacitance to buffer water stress. Karst species had high leaf bulk modulus, low leaf capacitance, and delayed fine root wilting. This study showed the general contribution of fine roots to the protection of the whole plant against underground water stress. Our findings highlight the importance of water storage in the leaves and fine roots of mangrove species and high tolerance to water deficit in the leaves of mangrove species and the fine roots of some karst species.

Complementary water and nutrient utilization of perianth structural units help maintain long floral lifespan in Dendrobium.

Most orchids have high ornamental value with long-lived flowers. However, the mechanisms by which orchids maintain floral longevity are poorly understood. Here, we hypothesized that floral longevity in Dendrobium is maintained by high resource investment and complementary water and nutrient utilization in different structural units of the perianth. To test this hypothesis, we determined which water- and nutrient-related traits are correlated with flower longevity in 23 Dendrobium species or cultivars, and examined variations of the related traits during flower development of one long-lived cultivar. We found that floral longevity was correlated with dry mass per unit area of perianths and total flower biomass, which indicates that maintaining floral longevity requires increased resource investment. During development of long-lived flowers, labella showed a high capacity for water storage and nutrient reutilization, which could partly remedy high water demand and biomass investment. Sepals and petals, in contrast, had stronger desiccation avoidance and higher metabolic activity with lower biomass investment. These findings indicate that Dendrobium flowers maintain longevity by complementary water and nutrient utilization strategies in the sepals, petals and labella, with labella consuming more water and nutrients to extend flower display, and sepals and petals using a more conservative strategy.

Diverse mangroves deviate from other angiosperms in their genome size, leaf cell size and cell packing density relationships.

BACKGROUND AND AIMS: While genome size limits the minimum sizes and maximum numbers of cells that can be packed into a given leaf volume, mature cell sizes can be substantially larger than their meristematic precursors and vary in response to abiotic conditions. Mangroves are iconic examples of how abiotic conditions can influence the evolution of plant phenotypes. METHODS: Here, we examined the coordination between genome size, leaf cell sizes, cell packing densities and leaf size in 13 mangrove species across four sites in China. Four of these species occurred at more than one site, allowing us to test the effect of climate on leaf anatomy. RESULTS: We found that genome sizes of mangroves were very small compared to other angiosperms, but, like other angiosperms, mangrove cells were always larger than the minimum size defined by genome size. Increasing mean annual temperature of a growth site led to higher packing densities of veins (Dv) and stomata (Ds) and smaller epidermal cells but had no effect on stomatal size. In contrast to other angiosperms, mangroves exhibited (1) a negative relationship between guard cell size and genome size; (2) epidermal cells that were smaller than stomata; and (3) coordination between Dv and Ds that was not mediated by epidermal cell size. Furthermore, mangrove epidermal cell sizes and packing densities covaried with leaf size. CONCLUSIONS: While mangroves exhibited coordination between veins and stomata and attained a maximum theoretical stomatal conductance similar to that of other angiosperms, the tissue-level tradeoffs underlying these similar relationships across species and environments were markedly different, perhaps indicative of the unique structural and physiological adaptations of mangroves to their stressful environments.

Correlations between leaf economics, mechanical resistance and drought tolerance across 41 cycad species.

BACKGROUND AND AIMS: We conducted a comprehensive analysis of the functional traits of leaves (leaflets) of cycads. The aim of this study was to clarify the functional divergence between the earlier origin Cycadaceae and the later differentiated Zamiaceae, and the differences in trait associations between cycads and angiosperms. METHODS: We selected 20 Cycadaceae species and 21 Zamiaceae species from the same cycad garden in South China, and measured their leaf structure, economic traits, mechanical resistance (Fp) and leaf water potential at the turgor loss point (πtlp). In addition, we compiled a dataset of geographical distribution along with climatic variables for these cycad species, and some leaf traits of tropical-sub-tropical angiosperm woody species from the literature for comparison. KEY RESULTS: The results showed significantly contrasting leaf trait syndromes between the two families, with Zamiaceae species exhibiting thicker leaves, higher carbon investments and greater Fp than Cycadaceae species. Leaf thickness (LT) and πtlp were correlated with mean climatic variables in their native distribution ranges, indicating their evolutionary adaptation to environmental conditions. Compared with the leaves of angiosperms, the cycad leaves were thicker and tougher, and more tolerant to desiccation. Greater Fp was associated with a higher structural investment in both angiosperms and cycads; however, cycads showed lower Fp at a given leaf mass per area or LT than angiosperms. Enhancement of Fp led to more negative πtlp in angiosperms, but the opposite trend was observed in cycads. CONCLUSIONS: Our results reveal that variations in leaf traits of cycads are mainly influenced by taxonomy and the environment of their native range. We also demonstrate similar leaf functional associations in terms of economics, but different relationships with regard to mechanics and drought tolerance between cycads and angiosperms. This study expands our understanding of the ecological strategies and likely responses of cycads to future climate change.

Hydraulic prediction of drought-induced plant dieback and top-kill depends on leaf habit and growth form.

Hydraulic failure caused by severe drought contributes to aboveground dieback and whole-plant death. The extent to which dieback or whole-plant death can be predicted by plant hydraulic traits has rarely been tested among species with different leaf habits and/or growth forms. We investigated 19 hydraulic traits in 40 woody species in a tropical savanna and their potential correlations with drought response during an extreme drought event during the El Niño-Southern Oscillation in 2015. Plant hydraulic trait variation was partitioned substantially by leaf habit but not growth form along a trade-off axis between traits that support drought tolerance versus avoidance. Semi-deciduous species and shrubs had the highest branch dieback and top-kill (complete aboveground death) among the leaf habits or growth forms. Dieback and top-kill were well explained by combining hydraulic traits with leaf habit and growth form, suggesting integrating life history traits with hydraulic traits will yield better predictions.

Increasing axial parenchyma fraction in the Malagasy Magnoliids facilitated the co-optimisation of hydraulic efficiency and safety.

The evolution of angiosperms was accompanied by the segregation and specialisation of their xylem tissues. This study aimed to determine whether the fraction and arrangement of parenchyma tissue influence the hydraulic efficiency-safety trade-off in the basal angiosperms. We examined xylem anatomical structure and hydraulic functioning of 28 woody species of Magnoliids in a tropical rainforest of Madagascar and reported, for the first time, quantitative measurements that support the relationship between vessel-to-xylem parenchyma connectivity and the hydraulic efficiency-safety trade-off. We also introduced a new measurement - the distance of species from the trade-off limit - to quantify the co-optimisation of hydraulic efficiency and safety. Although the basal angiosperms in this study had low hydraulic conductivity and safety, species with higher axial parenchyma fraction (APf) had significantly higher hydraulic conductivity. Hydraulic efficiency-safety optimisation was accompanied by higher APf and vessel-to-axial parenchyma connectivity. Conversely, species exhibiting high ray parenchyma fraction and high vessel-to-ray connectivity had lower Ks and were further away from the hydraulic trade-off limit line. Our results provide evidence that axial parenchyma fraction and paratracheal arrangement are associated with both enhanced hydraulic efficiency and safety.

Correlations between allocation to foliar phosphorus fractions and maintenance of photosynthetic integrity in six mangrove populations as affected by chilling.

Chilling restrains the distribution of mangroves. We tested whether foliar phosphorus (P) fractions and gene expression are associated with cold tolerance in mangrove species. We exposed seedlings of six mangrove populations from different latitudes to favorable, chilling and recovery treatments, and measured their foliar P concentrations and fractions, photochemistry, nighttime respiration, and gene expression. A Kandelia obovata (KO; 26.45°N) population completely and a Bruguiera gymnorhiza (Guangxi) (BGG; 21.50°N) population partially (30%) survived chilling. Avicennia marina (24.29°N), and other B. gymnorhiza (26.66°N, 24.40°N, and 19.62°N) populations died after chilling. Photosystems of KO and photosystem I of BGG were least injured. During chilling, leaf P fractions, except nucleic acid P in three populations, declined and photoinhibition and nighttime respiration increased in all populations, with the greatest impact in B. gymnorhiza. Leaf nucleic acid P was positively correlated with photochemical efficiency during recovery and nighttime respiration across populations for each treatment. Relatively high concentrations of nucleic acid P and metabolite P were associated with stronger chilling tolerance in KO. Bruguiera gymnorhiza exhibited relatively low concentrations of organic P in favorable and chilling conditions, but its partially survived population showed stronger compensation in nucleic acid P and Pi concentrations and gene expression during recovery.

No gas source, no problem: Proximity to pre-existing embolism and segmentation affect embolism spreading in angiosperm xylem by gas diffusion.

Embolism spreading in dehydrating angiosperm xylem is driven by gas movement between embolized and sap-filled conduits. Here we examine how the proximity to pre-existing embolism and hydraulic segmentation affect embolism propagation. Based on the optical method, we compare xylem embolism resistance between detached leaves and leaves attached to branches, and between intact leaves and leaves with cut minor veins, for six species. Embolism resistance of detached leaves was significantly lower than that of leaves attached to stems, except for two species, with all vessels ending in their petioles. Cutting of minor veins showed limited embolism spreading in minor veins near the cuts prior to major veins. Moreover, despite strong agreement in the overall embolism resistance of detached leaves between the optical and pneumatic method, minor differences were observed during early stages of embolism formation. We conclude that embolism resistance may represent a relative trait due to an open-xylem artefact, with embolism spreading possibly affected by the proximity and connectivity to pre-existing embolism as a gas source, while hydraulic segmentation prevents such artefact. Since embolism formation may not rely on a certain pressure difference threshold between functional and embolized conduits, we speculate that embolism is facilitated by pressure-driven gas diffusion across pit membranes.

Co-ordination between leaf biomechanical resistance and hydraulic safety across 30 sub-tropical woody species.

BACKGROUND AND AIMS: Leaf biomechanical resistance protects leaves from biotic and abiotic damage. Previous studies have revealed that enhancing leaf biomechanical resistance is costly for plant species and leads to an increase in leaf drought tolerance. We thus predicted that there is a functional correlation between leaf hydraulic safety and biomechanical characteristics. METHODS: We measured leaf morphological and anatomical traits, pressure-volume parameters, maximum leaf hydraulic conductance (Kleaf-max), leaf water potential at 50 % loss of hydraulic conductance (P50leaf), leaf hydraulic safety margin (SMleaf), and leaf force to tear (Ft) and punch (Fp) of 30 co-occurring woody species in a sub-tropical evergreen broadleaved forest. Linear regression analysis was performed to examine the relationships between biomechanical resistance and other leaf hydraulic traits. KEY RESULTS: We found that higher Ft and Fp values were significantly associated with a lower (more negative) P50leaf and a larger SMleaf, thereby confirming the correlation between leaf biomechanical resistance and hydraulic safety. However, leaf biomechanical resistance showed no correlation with Kleaf-max, although it was significantly and negatively correlated with leaf outside-xylem hydraulic conductance. In addition, we also found that there was a significant correlation between biomechanical resistance and the modulus of elasticity by excluding an outlier. CONCLUSIONS: The findings of this study reveal leaf biomechanical-hydraulic safety correlation in sub-tropical woody species.

Leaf hydraulic safety margin and safety-efficiency trade-off across angiosperm woody species.

Leaf hydraulic conductance and the vulnerability to water deficits have profound effects on plant distribution and mortality. In this study, we compiled a leaf hydraulic trait dataset with 311 species-at-site combinations from biomes worldwide. These traits included maximum leaf hydraulic conductance (Kleaf), water potential at 50% loss of Kleaf (P50leaf), and minimum leaf water potential (Ψmin). Leaf hydraulic safety margin (HSMleaf) was calculated as the difference between Ψmin and P50leaf. Our results indicated that 70% of the studied species had a narrow HSMleaf (less than 1 MPa), which was consistent with the global pattern of stem hydraulic safety margin. There was a positive relationship between HSMleaf and aridity index (the ratio of mean annual precipitation to potential evapotranspiration), as species from humid sites tended to have larger HSMleaf. We found a significant relationship between Kleaf and P50leaf across global angiosperm woody species and within each of the different plant groups. This global analysis of leaf hydraulic traits improves our understanding of plant hydraulic response to environmental change.

Hydraulic traits are more diverse in flowers than in leaves.

Maintaining water balance has been a critical constraint shaping the evolution of leaf form and function. However, flowers, which are heterotrophic and relatively short-lived, may not be constrained by the same physiological and developmental factors. We measured physiological parameters derived from pressure-volume curves for leaves and flowers of 22 species to characterize the diversity of hydraulic traits in flowers and to determine whether flowers are governed by the same constraints as leaves. Compared with leaves, flowers had high saturated water content, which was a strong predictor of hydraulic capacitance in both leaves and flowers. Principal component analysis revealed that flowers occupied a different region of multivariate trait space than leaves and that hydraulic traits are more diverse in flowers than in leaves. Without needing to maintain high rates of transpiration, flowers rely on other hydraulic traits, such as high hydraulic capacitance, to maintain turgor pressure. As a result, instead of employing a metabolically expensive but durable carbon (C)-based skeleton, flowers may rely predominantly on a metabolically cheaper, hydrostatic skeleton to keep their structures on display for pollinators, which has important implications for both the costs of reproduction and the biomechanical performance of flowers, particularly during drought.

The effects of intervessel pit characteristics on xylem hydraulic efficiency and photosynthesis in hemiepiphytic and non-hemiepiphytic Ficus species.

Xylem vulnerability to cavitation and hydraulic efficiency are directly linked to fine-scale bordered pit features in water-conducting cells of vascular plants. However, it is unclear how pit characteristics influence water transport and carbon economy in tropical species. The primary aim of this study was to evaluate functional implications of changes in pit characteristics for water relations and photosynthetic traits in tropical Ficus species with different growth forms (i.e. hemiepiphytic and non-hemiepiphytic) grown under common conditions. Intervessel pit characteristics were measured using scanning electron microscopy in five hemiepiphytic and five non-hemiepiphytic Ficus species to determine whether these traits were related to hydraulics, leaf photosynthesis, stomatal conductance and wood density. Ficus species varied greatly in intervessel pit structure, hydraulic conductivity and leaf physiology, and clear differences were observed between the two growth forms. The area and diameter of pit aperture were negatively correlated with sapwood-specific hydraulic conductivity, mass-based net assimilation rate, stomatal conductance (gs ), intercellular CO2 concentration (Ci ) and the petiole vessel lumen diameters (Dv ), but positively correlated with wood density. Pit morphology was only negatively correlated with sapwood- and leaf-specific hydraulic conductivity and Dv . Pit density was positively correlated with gs , Ci and Dv , but negatively with intrinsic leaf water-use efficiency. Pit and pit aperture shape were not significantly correlated with any of the physiological traits. These findings indicate a significant role of pit characteristics in xylem water transport, carbon assimilation and ecophysiological adaptation of Ficus species in tropical rain forests.

Is xylem of angiosperm leaves less resistant to embolism than branches? Insights from microCT, hydraulics, and anatomy.

According to the hydraulic vulnerability segmentation hypothesis, leaves are more vulnerable to decline of hydraulic conductivity than branches, but whether stem xylem is more embolism resistant than leaves remains unclear. Drought-induced embolism resistance of leaf xylem was investigated based on X-ray microcomputed tomography (microCT) for Betula pendula, Laurus nobilis, and Liriodendron tulipifera, excluding outside-xylem, and compared with hydraulic vulnerability curves for branch xylem. Moreover, bordered pit characters related to embolism resistance were investigated for both organs. Theoretical P50 values (i.e. the xylem pressure corresponding to 50% loss of hydraulic conductance) of leaves were generally within the same range as hydraulic P50 values of branches. P50 values of leaves were similar to branches for L. tulipifera (-2.01 versus -2.10 MPa, respectively), more negative for B. pendula (-2.87 versus -1.80 MPa), and less negative for L. nobilis (-6.4 versus -9.2 MPa). Despite more narrow conduits in leaves than branches, mean interconduit pit membrane thickness was similar in both organs, but significantly higher in leaves of B. pendula than in branches. This case study indicates that xylem shows a largely similar embolism resistance across leaves and branches, although differences both within and across organs may occur, suggesting interspecific variation with regard to the hydraulic vulnerability segmentation hypothesis.

The physiological cold tolerance of warm-climate plants is correlated with their latitudinal range limit.

Plants are moving poleward and upward in response to climate warming. However, such movements lag behind the expanding warming front for many reasons, including the impediment of plant movement caused by unusual cold events. In this study, we measured the maximum photochemical efficiency of photosystem II (Fv/Fm) in 101 warm-climate angiosperm species to assess their cold tolerance at the end of a severe chilling period of 49 days in a southern subtropical region (Nanning) in China. We found that 36 of the 101 species suffered from chilling-induced physiological injury, with predawn Fv/Fm values of less than 0.7. There was a significant exponential relationship between the predawn Fv/Fm and northern latitudinal limit of a species; species with a lower latitudinal limit suffered more. Our results suggest that the range limits of warm-climate plants are potentially influenced by their physiological sensitivity to chilling temperatures and that their poleward movement might be impeded by extreme cold events. The quick measurement of Fv/Fm is useful for assessing the cold tolerance of plants, providing valuable information for modelling species range shifts under changing climate conditions and species selection for horticultural management and urban landscape design.

Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy.

Although fine roots are important components of the global carbon cycle, there is limited understanding of root structure-function relationships among species. We determined whether root respiration rate and decomposability, two key processes driving carbon cycling but always studied separately, varied with root morphological and chemical traits, in a coordinated way that would demonstrate the existence of a root economics spectrum (RES). Twelve traits were measured on fine roots (diameter ≤ 2 mm) of 74 species (31 graminoids and 43 herbaceous and dwarf shrub eudicots) collected in three biomes. The findings of this study support the existence of a RES representing an axis of trait variation in which root respiration was positively correlated to nitrogen concentration and specific root length and negatively correlated to the root dry matter content, lignin : nitrogen ratio and the remaining mass after decomposition. This pattern of traits was highly consistent within graminoids but less consistent within eudicots, as a result of an uncoupling between decomposability and morphology, and of heterogeneity of individual roots of eudicots within the fine-root pool. The positive relationship found between root respiration and decomposability is essential for a better understanding of vegetation-soil feedbacks and for improving terrestrial biosphere models predicting the consequences of plant community changes for carbon cycling.

Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species.

The evolution of lignified xylem allowed for the efficient transport of water under tension, but also exposed the vascular network to the risk of gas emboli and the spread of gas between xylem conduits, thus impeding sap transport to the leaves. A well-known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water). We tested this safety-efficiency hypothesis in branch xylem across 335 angiosperm and 89 gymnosperm species. Safety was considered at three levels: the xylem water potentials where 12%, 50% and 88% of maximal conductivity are lost. Although correlations between safety and efficiency were weak (r(2)  < 0.086), no species had high efficiency and high safety, supporting the idea for a safety-efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated (r(2)  < 0.02 in most cases) with higher wood density, lower leaf- to sapwood-area and shorter stature. There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem.