Comparative venation costs of monocotyledon and dicotyledon species in the eastern Colorado steppe.

MAIN CONCLUSION: Leaf vein network cost (total vein surface area per leaf volume) for major veins and vascular bundles did not differ between monocot and dicot species in 21 species from the eastern Colorado steppe. Dicots possessed significantly larger minor vein networks than monocots. Across the tree of life, there is evidence that dendritic vascular transport networks are optimized, balancing maximum speed and integrity of resource delivery with minimal resource investment in transport and infrastructure. Monocot venation, however, is not dendritic, and remains parallel down to the smallest vein orders with no space-filling capillary networks. Given this departure from the "optimized" dendritic network, one would assume that monocots are operating at a significant energetic disadvantage. In this study, we investigate whether monocot venation networks bear significantly greater carbon/construction costs per leaf volume than co-occurring dicots in the same ecosystem, and if so, what physiological or ecological advantage the monocot life form possesses to compensate for this deficit. Given that venation networks could also be optimized for leaf mechanical support or provide herbivory defense, we measured the vascular system of both monocot and dicots at three scales to distinguish between leaf investment in mechanical support (macroscopic vein), total transport and capacitance (vascular bundle), or exclusively water transport (xylem) for both parallel and dendritic venation networks. We observed that vein network cost (total vein surface area per leaf volume) for major veins and vascular bundles was not significantly different between monocot species and dicot species. Dicots, however, possess significantly larger minor vein networks than monocots. The 19 species subjected to gas-exchange measurement in the field displayed a broad range of Amax and but demonstrated no significant relationships with any metric of vascular network size in major or minor vein classes. Given that monocots do not seem to display any leaf hydraulic disadvantage relative to dicots, it remains an important research question why parallel venation (truly parallel, down to the smallest vessels) has not arisen more than once in the history of plant evolution.

Coupled hydraulics and carbon economy underlie age-related growth decline and revitalisation of sand-fixing shrubs after crown removal.

Crown removal revitalises sand-fixing shrubs that show declining vigour with age in drought-prone environments; however, the underlying mechanisms are poorly understood. Here, we addressed this knowledge gap by comparing the growth performance, xylem hydraulics and plant carbon economy across different plant ages (10, 21 and 33 years) and treatments (control and crown removal) using a representative sand-fixing shrub (Caragana microphylla Lam.) in northern China. We found that growth decline with plant age was accompanied by simultaneous decreases in soil moisture, plant hydraulic efficiency and photosynthetic capacity, suggesting that these interconnected changes in plant water relations and carbon economy were responsible for this decline. Following crown removal, quick resprouting, involving remobilisation of root nonstructural carbohydrate reserves, contributed to the reconstruction of an efficient hydraulic system and improved plant carbon status, but this became less effective in older shrubs. These age-dependent effects of carbon economy and hydraulics on plant growth vigour provide a mechanistic explanation for the age-related decline and revitalisation of sand-fixing shrubs. This understanding is crucial for the development of suitable management strategies for shrub plantations constructed with species having the resprouting ability and contributes to the sustainability of ecological restoration projects in water-limited sandy lands.

Energy costs of salinity tolerance in crop plants: night-time transpiration and growth.

Plants grow and transpire during the night. The aim of the present work was to assess the relative flows of carbon, water and solutes, and the energy involved, in sustaining night-time transpiration and leaf expansive growth under control and salt-stress conditions. Published and unpublished data were used, for barley plants grown in presence of 0.5-1 mM NaCl (control) and 100 mM NaCl. Night-time leaf growth presents a more efficient use of taken-up water compared with day-time growth. This efficiency increases several-fold with salt stress. Night-time transpiration cannot be supported entirely through osmotically driven uptake of water through roots under salt stress. Using a simple three- (root medium/cytosol/vacuole) compartment approach, the energy required to support cell expansion during the night is in the lower percentage region (0.03-5.5%) of the energy available through respiration, under both, control and salt-stress conditions. Use of organic (e.g. hexose equivalents) rather than inorganic (e.g. Na+ , Cl- , K+ ) solutes for generation of osmotic pressure in growing cells, increases the energy demand by orders of magnitude, yet requires only a small portion of carbon assimilated during the day. Night-time transpiration and leaf expansive growth should be considered as a potential acclimation mechanism to salinity.

Leaf economics and plant hydraulics drive leaf : wood area ratios.

Biomass and area ratios between leaves, stems and roots regulate many physiological and ecological processes. The Huber value Hv (sapwood area/leaf area ratio) is central to plant water balance and drought responses. However, its coordination with key plant functional traits is poorly understood, and prevents developing trait-based prediction models. Based on theoretical arguments, we hypothesise that global patterns in Hv of terminal woody branches can be predicted from variables related to plant trait spectra, that is plant hydraulics and size and leaf economics. Using a global compilation of 1135 species-averaged Hv , we show that Hv varies over three orders of magnitude. Higher Hv are seen in short small-leaved low-specific leaf area (SLA) shrubs with low Ks in arid relative to tall large-leaved high-SLA trees with high Ks in moist environments. All traits depend on climate but climatic correlations are stronger for explanatory traits than Hv . Negative isometry is found between Hv and Ks , suggesting a compensation to maintain hydraulic supply to leaves across species. This work identifies the major global drivers of branch sapwood/leaf area ratios. Our approach based on widely available traits facilitates the development of accurate models of above-ground biomass allocation and helps predict vegetation responses to drought.

Studies on gas exchange in the meadow spittlebug, Philaenus spumarius: the metabolic cost of feeding on, and living in, xylem sap.

Spittlebugs (superfamily Cercopoidea) live within a mass of frothy, spittle-like foam that is produced as a by-product of their xylem-feeding habits. The wet spittle represents a unique respiratory environment for an insect, potentially acting either as a reserve of trapped oxygen (O2) or as a significant barrier to O2 diffusion from the surrounding atmosphere. Feeding on xylem sap under tension is also assumed to be energetically expensive, potentially placing further constraints on their gas exchange. To understand the respiratory strategies used by spittlebugs, this study measured the PO2  within the spittle of the meadow spittlebug, Philaenus spumarius, as well as the non-feeding metabolic rate (RMR) and respiratory quotient (RQ) of both nymphs and adults. The metabolic rate of nymphs feeding on xylem was also measured. In separate experiments, the ability of a nymph to obtain O2 from bubbles while submerged in foam was determined using a glass microscope slide coated in an O2-sensitive fluorophore. We determined that P. spumarius breathes atmospheric O2 by extending the tip of its abdomen outside of its spittle, rather than respiring the O2 trapped in air bubbles within the foam. However, spittlebugs can temporarily use these air bubbles to breathe when forcibly submerged. V̇O2  and V̇CO2  did not differ statistically within life stages, giving a RQ of 0.92 for nymphs and 0.95 for adults. Feeding on xylem was found to increase the nymphs' V̇CO2  by only 20% above their RMR. From this cost of feeding, cibarial pump pressures were estimated to be between -0.05 and -0.26 MPa.

Xylem hydraulic safety and construction costs determine tropical tree growth.

Faster growth in tropical trees is usually associated with higher mortality rates, but the mechanisms underlying this relationship are poorly understood. In this study, we investigate how tree growth patterns are linked with environmental conditions and hydraulic traits, by monitoring the cambial growth of 9 tropical cloud forest tree species coupled with numerical simulations using an optimization model. We find that fast-growing trees have lower xylem safety margins than slow-growing trees and this pattern is not necessarily linked to differences in stomatal behaviour or environmental conditions when growth occurs. Instead, fast-growing trees have xylem vessels that are more vulnerable to cavitation and lower density wood. We propose the growth - xylem vulnerability trade-off represents a wood hydraulic economics spectrum similar to the classic leaf economic spectrum, and show through numerical simulations that this trade-off can emerge from the coordination between growth rates, wood density, and xylem vulnerability to cavitation. Our results suggest that vulnerability to hydraulic failure might be related with the growth-mortality trade-off in tropical trees, determining important life history differences. These findings are important in furthering our understanding of xylem hydraulic functioning and its implications on plant carbon economy.

The cost of avoiding freezing in stems: trade-off between xylem resistance to cavitation and supercooling capacity in woody plants.

Stems and leaves of Olea europaea L. (olive) avoid freezing damage by substantial supercooling during the winter season. Physiological changes during acclimation to low temperatures were studied in five olive cultivars. Water relations and hydraulic traits, ice nucleation temperature (INT) and temperatures resulting in 50% damage (LT50) were determined. All cultivars showed a gradual decrease in INT and LT50 from the dry and warm summer to the wet and cold winter in Patagonia, Argentina. During acclimation to low temperatures there was an increase in leaf cell wall rigidity and stomatal conductance (gs), as well as a decrease in leaf apoplastic water content, leaf water potential (Ψ), sap flow and stem hydraulic conductivity (ks). More negative Ψ as a consequence of high gs and detrimental effects of low temperatures on root activity resulted in a substantial loss of ks due to embolism formation. Seasonal stem INT decrease from summer to winter was directly related to the xylem resistance to cavitation, determined by the loss of ks across cultivars. Thus the loss of freezable water in xylem vessels by embolisms increased stem supercooling capacity and delayed ice propagation from stems to the leaves. For the first time, a trade-off between xylem resistance to cavitation and stem and leaf supercooling capacity was observed in plants that avoid extracellular freezing by permanent supercooling. The substantial loss of hydraulic function in olive cultivar stems by embolism formation with their high repair costs are compensated by avoiding plant damage at very low subzero temperatures.

Interplay of growth rate and xylem plasticity for optimal coordination of carbon and hydraulic economies in Fraxinus ornus trees.

Efficient leaf water supply is fundamental for assimilation processes and tree growth. Renovating the architecture of the xylem transport system requires an increasing carbon investment while growing taller, and any deficiency of carbon availability may result in increasing hydraulic constraints to water flow. Therefore, plants need to coordinate carbon assimilation and biomass allocation to guarantee an efficient and safe long-distance transport system. We tested the hypothesis that reduced branch elongation rates together with carbon-saving adjustments of xylem anatomy hydraulically compensate for the reduction in biomass allocation to xylem. We measured leaf biomass, hydraulic and anatomical properties of wood segments along the main axis of branches in 10 slow growing (SG) and 10 fast growing (FG) Fraxinus ornus L. trees. Branches of SG trees had five times slower branch elongation rate (7 vs 35 cm year-1), and produced a higher leaf biomass (P < 0.0001) and thinner xylem rings with fewer but larger vessels (P < 0.0001). On the contrary, we found no differences between SG and FG trees in terms of leaf-specific conductivity (P > 0.05) and xylem safety (Ψ50 ≈ -3.2 MPa). Slower elongation rate coupled with thinner annual rings and larger vessels allows the reduction of carbon costs associated with growth, while maintaining similar leaf-specific conductivity and xylem safety.

Linking xylem hydraulic conductivity and vulnerability to the leaf economics spectrum--a cross-species study of 39 evergreen and deciduous broadleaved subtropical tree species.

While the fundamental trade-off in leaf traits related to carbon capture as described by the leaf economics spectrum is well-established among plant species, the relationship of the leaf economics spectrum to stem hydraulics is much less known. Since carbon capture and transpiration are coupled, a close connection between leaf traits and stem hydraulics should be expected. We thus asked whether xylem traits that describe drought tolerance and vulnerability to cavitation are linked to particular leaf traits. We assessed xylem vulnerability, using the pressure sleeve technique, and anatomical xylem characteristics in 39 subtropical tree species grown under common garden conditions in the BEF-China experiment and tested for correlations with traits related to the leaf economics spectrum as well as to stomatal control, including maximum stomatal conductance, vapor pressure deficit at maximum stomatal conductance and vapor pressure deficit at which stomatal conductance is down-regulated. Our results revealed that specific xylem hydraulic conductivity and cavitation resistance were closely linked to traits represented in the leaf economic spectrum, in particular to leaf nitrogen concentration, as well as to log leaf area and leaf carbon to nitrogen ratio but not to any parameter of stomatal conductance. The study highlights the potential use of well-known leaf traits from the leaf economics spectrum to predict plant species' drought resistance.

Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences.

Leaf hydraulic conductance (K(leaf) ) and vulnerability constrain plant productivity, but no clear trade-off between these fundamental functional traits has emerged in previous studies. We measured K(leaf) on a leaf area (K(leaf_area)) and mass basis (K(leaf_mass)) in six woody angiosperms, and compared these values with species' distribution and leaf tolerance to dehydration in terms of P(50), that is, the leaf water potential inducing 50% loss of K(leaf) . We also measured several morphological and anatomical traits associated with carbon investment in leaf construction and water transport efficiency. Clear relationships emerged between K(leaf_mass), P(50), and leaf mass per unit area (LMA), suggesting that increased tolerance to hydraulic dysfunction implies increased carbon costs for leaf construction and water use. Low P(50) values were associated with narrower and denser vein conduits, increased thickness of conduit walls, and increased vein density. This, in turn, was associated with reduced leaf surface area. Leaf P(50) was closely associated with plants' distribution over a narrow geographical range, suggesting that this parameter contributes to shaping vegetation features. Our data also highlight the carbon costs likely to be associated with increased leaf tolerance to hydraulic dysfunction, which confers on some species the ability to thrive under reduced water availability but decreases their competitiveness in high-resource habitats.

A model of heat transfer in sapwood and implications for sap flux density measurements using thermal dissipation probes.

A variety of thermal approaches are used to estimate sap flux density in stems of woody plants. Models have proved valuable tools for interpreting the behavior of heat pulse, heat balance and heat field deformation techniques, but have seldom been used to describe heat transfer dynamics for the heat dissipation method. Therefore, to better understand the behavior of heat dissipation probes, a model was developed that takes into account the thermal properties of wood, the physical dimensions and thermal characteristics of the probes, and the conductive and convective heat transfer that occurs due to water flow in the sapwood. Probes were simulated as aluminum tubes 20 mm in length and 2 mm in diameter, whereas sapwood, heartwood and bark each had a density and water fraction that determined their thermal properties. Base simulations assumed a constant sap flux density with sapwood depth and no wounding or physical disruption of xylem beyond the 2 mm diameter hole drilled for probe installation. Simulations across a range of sap flux densities showed that the dimensionless quantity k [defined as (ΔT(m) -ΔT)/ΔT, where ΔT(m) is the temperature differential (ΔT) between the heated and unheated probe under zero-flow conditions] was dependent on the thermal conductivity of the sapwood. The relationship between sap flux density and k was also sensitive to radial gradients in sap flux density and to xylem disruption near the probe. Monte Carlo analysis in which 1000 simulations were conducted while simultaneously varying thermal conductivity and wound diameter revealed that sap flux density and k showed considerable departure from the original calibration equation used with this technique. The departure was greatest for variation in sap flux density typical of ring-porous species. Depending on the specific combination of thermal conductivity and wound diameter, use of the original calibration equation resulted in an 81% under- to 48% overestimation of sap flux density at modest flux rates. Future studies should verify these simulations and assess their utility in estimating sap flux density for this widely used technique.

A carbon cost-gain model explains the observed patterns of xylem safety and efficiency.

Efficient water transport from the soil to the leaves is essential for plant function, while building and maintaining the water transport structure in the xylem require a major proportion of the assimilated carbon of the tree. Xylem transport also faces additional challenges as water in the xylem is under tension and therefore cavitation cannot be completely avoided. We constructed a model that calculates the xylem structure that maximizes carbon-use efficiency while simultaneously taking into account pit structure in increasing the resistance to water transport and constricting the spreading of embolisms. The optimal xylem structure predicted by the model was found to correspond well to the generally observed trends: xylem conduits grew in size from the apex towards the base while simultaneously decreasing in number, and vulnerability to cavitation increased with conduit size. These trends were caused primarily by the axial water potential gradient in the xylem. The pits have to be less porous near the apex where water potential is lower to restrict the spreading of embolisms, while whole-plant carbon-use efficiency demands that conduit size decreases and conduit number increases simultaneously. The model predictions remained qualitatively the same regardless of the exact optimality criterion used for defining carbon-use efficiency.