Stomatal dynamics are limited by leaf hydraulics in ferns and conifers: results from simultaneous measurements of liquid and vapour fluxes in leaves

Stomatal responsiveness to vapour pressure deficit (VPD) results in continuous regulation of daytime gas‐exchange directly influencing leaf water status and carbon gain. Current models can reasonably predict steady‐state stomatal conductance (g_s) to changes in VPD but the g_s dynamics between steady‐states are poorly known. Here, we used a diverse sample of conifers and ferns to show that leaf hydraulic architecture, in particular leaf capacitance, has a major role in determining the g_s response time to perturbations in VPD. By using simultaneous measurements of liquid and vapour fluxes into and out of leaves, the in situ fluctuations in leaf water balance were calculated and appeared to be closely tracked by changes in g_s thus supporting a passive model of stomatal control. Indeed, good agreement was found between observed and predicted g_s when using a hydropassive model based on hydraulic traits. We contend that a simple passive hydraulic control of stomata in response to changes in leaf water status provides for efficient stomatal responses to VPD in ferns and conifers, leading to closure rates as fast or faster than those seen in most angiosperms.     

The 'hydrology' of leaves: co-ordination of structure and function in temperate woody species

The hydraulic conductance of the leaf lamina (K_lamina) substantially constrains whole‐plant water transport, but little is known of its association with leaf structure and function. K_lamina was measured for sun and shade leaves of six woody temperate species growing in moist soil, and tested for correlation with the prevailing leaf irradiance, and with 22 other leaf traits. K_lamina varied from 7.40 × 10^?5 kg m^?2 s^?1 MPa^?1 for Acer saccharum shade leaves to 2.89 × 10^?4 kg m^?2 s^?1 MPa^?1 for Vitis labrusca sun leaves. Tree sun leaves had 15–67% higher K_lamina than shade leaves. K_lamina was co‐ordinated with traits associated with high water flux, including leaf irradiance, petiole hydraulic conductance, guard cell length, and stomatal pore area per lamina area. K_lamina was also co‐ordinated with lamina thickness, water storage capacitance, 1/mesophyll water transfer resistance, and, in five of the six species, with lamina perimeter/area. However, for the six species, K_lamina was independent of inter‐related leaf traits including leaf dry mass per area, density, modulus of elasticity, osmotic potential, and cuticular conductance. K_lamina was thus co‐ordinated with structural and functional traits relating to liquid‐phase water transport and to maximum rates of gas exchange, but independent of other traits relating to drought tolerance and to aspects of carbon economy.     

Impact of light quality on leaf and shoot hydraulic properties: a case study in silver birch (Betula pendula)

Responses of leaf and shoot hydraulic conductance to light quality were examined on shoots of silver birch (Betula pendula), cut from lower (‘shade position’) and upper thirds of the crowns (‘sun position’) of trees growing in a natural temperate forest stand. Hydraulic conductances of leaf blades (K_lb), petioles (K_P) and branches (i.e. leafless stem; K_B) were determined using a high pressure flow meter in steady state mode. The shoots were exposed to photosynthetic photon flux density of 200–250 µmol m^?2 s^?1 using white, blue or red light. K_lb depended significantly on both light quality and canopy position (P < 0.001), K_B on canopy position (P < 0.001) and exposure time (P = 0.014), and none of the three factors had effect on K_P. The highest values of K_lb were recorded under the blue light (3.63 and 3.13 × 10^?4 kg m^?2 MPa^?1 s^?1 for the sun and shade leaves, respectively), intermediate values under white light (3.37 and 2.46 × 10^?4 kg m^?2 MPa^?1 s^?1, respectively) and lowest values under red light (2.83 and 2.02 × 10^?4 kg m^?2 MPa^?1 s^?1, respectively). Light quality has an important impact on leaf hydraulic properties, independently of light intensity or of total light energy, and the specific light receptors involved in this response require identification. Given that natural canopy shade depletes blue and red light, K_lb may be decreased both by reduced fluence and shifts in light spectra, indicating the need for studies of the natural heterogeneity of K_lb within and under canopies, and its impacts on gas exchange.     

Leaf teeth, transpiration and the retrieval of apoplastic solutes in balsam poplar

The rapid flow of the transpiration stream through major veins to leaf teeth was followed in leaves of Populus balsamifera L., using the tracer sulphorhodamine G (SR), which probes for cells with H⁺-extrusion pumps. The tracer accumulated quickly in the hydathodes of the teeth. It was shown by freeze-substitution and anhydrous processing that SR was taken up by phloem parenchyma and epithem cells of the hydathode. When ¹⁴C-labelled aspartate was fed to the leaves in the transpiration stream, it also was taken up most strongly by the same phloem parenchyma and epithem cells. It is proposed that one function of the hydathodes in leaf teeth is the retrieval of solutes from the transpiration stream.     

Foliar water uptake in Amazonian trees: Evidence and consequences

The absorption of atmospheric water directly into leaves enables plants to alleviate the water stress caused by low soil moisture, hydraulic resistance in the xylem and the effect of gravity on the water column, while enabling plants to scavenge small inputs of water from leaf‐wetting events. By increasing the availability of water, and supplying it from the top of the canopy (in a direction facilitated by gravity), foliar uptake (FU) may be a significant process in determining how forests interact with climate, and could alter our interpretation of current metrics for hydraulic stress and sensitivity. FU has not been reported for lowland tropical rainforests; we test whether FU occurs in six common Amazonian tree genera in lowland Amazônia, and make a first estimation of its contribution to canopy–atmosphere water exchange. We demonstrate that FU occurs in all six genera and that dew‐derived water may therefore be used to “pay” for some morning transpiration in the dry season. Using meteorological and canopy wetness data, coupled with empirically derived estimates of leaf conductance to FU (k_fu), we estimate that the contribution by FU to annual transpiration at this site has a median value of 8.2% (103 mm/year) and an interquartile range of 3.4%–15.3%, with the biggest sources of uncertainty being k_fu and the proportion of time the canopy is wet. Our results indicate that FU is likely to be a common strategy and may have significant implications for the Amazon carbon budget. The process of foliar water uptake may also have a profound impact on the drought tolerance of individual Amazonian trees and tree species, and on the cycling of water and carbon, regionally and globally.     

Isometric partitioning of hydraulic conductance between leaves and stems: balancing safety and efficiency in different growth forms and habitats

Recent advances in modelling the architecture and function of the plant hydraulic network have led to improvements in predicting and interpreting the consequences of functional trait variation on CO₂ uptake and water loss. We build upon one such model to make novel predictions for scaling of the total specific hydraulic conductance of leaves and shoots (k_L and k_SH, respectively) and variation in the partitioning of hydraulic conductance. Consistent with theory, we observed isometric (slope = 1) scaling between k_L and k_SH across several independently collected datasets and a lower ratio of k_L and k_SH, termed the leaf‐to‐shoot conductance ratio (C_LSCR), in arid environments and in woody species. Isometric scaling of k_L and k_SH supports the concept that hydraulic design is coordinated across the plant. We propose that C_LSCR is an important adaptive trait that represents the trade‐off between efficiency and safety at the scale of the whole plant.     

基于树干液流和土壤-叶片水势梯度分析荷木干湿季整树水分利用特征

运用Granier热消散探针连续监测荷木的树干液流,于2009年的湿季(8月)和干季(11月)选择天气晴朗的3d测定叶片水势,同步连续监测林冠上方光合有效辐射、土壤含水量、气温和空气相对湿度.结果表明:干湿季下荷木树干液流存在显著差异,此外,土壤水势和液流有较好的相关性,且干季时的相关性更好;荷木的叶面积/边材面积比值平均为(0.416±0.033)m2·cm-2,并与树高呈指数函数下降关系;随着11月土壤水势下降,荷木的整树水力导度和午间叶片水势也有所下降,但不明显;对叶片水势和整树蒸腾进行回归分析,二者之间呈二次多项式关系(P＜0.01),叶片水势并非无限制下降;结果还表明,大气水汽压亏缺(D)和叶片水势呈负相关,这是否空气温度和相对湿度或共同作用影响叶片水势,需要进一步研究.     

Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species

Efficient conduction of water inside leaves is essential for leaf function, yet the hydraulic-mediated impact of drought on gas exchange remains poorly understood. Here we examine the decline and subsequent recovery of leaf water potential ( Ψ _leaf), leaf hydraulic conductance ( K _leaf), and midday transpiration ( E ) in four temperate woody species exposed to controlled drought conditions ranging from mild to lethal. During drought the vulnerability of K _leaf to declining Ψ _leaf varied greatly among the species sampled. Following drought, plants were rewatered and the rate of E and K _leaf recovery was found to be strongly dependent on the severity of the drought imposed. Gas exchange recovery was strongly correlated with the relatively slow recovery of K _leaf for three of the four species, indicating conformity to a hydraulic-stomatal limitation model of plant recovery. However, there was also a shift in the sensitivity of stomata to Ψ _leaf suggesting that the plant hormone abscisic acid may be involved in limiting the rate of stomatal reopening. The level of drought tolerance varied among the four species and was correlated with leaf hydraulic vulnerability. These results suggest that species-specific variation in hydraulic properties plays a fundamental role in steering the dynamic response of plants during recovery.     

Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima

* The hydraulic plumbing of vascular plant leaves varies considerably between major plant groups both in the spatial organization of veins, as well as their anatomical structure. * Five conifers, three ferns and 12 angiosperm trees were selected from tropical and temperate forests to investigate whether the profound differences in foliar morphology of these groups lead to correspondingly profound differences in leaf hydraulic efficiency. * We found that angiosperm leaves spanned a range of leaf hydraulic conductance from 3.9 to 36 mmol m2 s-1 MPa-1, whereas ferns (5.9-11.4 mmol m-2 s-1 MPa-1) and conifers (1.6-9.0 mmol m-2 s-1 MPa-1) were uniformly less conductive to liquid water. Leaf hydraulic conductance (Kleaf) correlated strongly with stomatal conductance indicating an internal leaf-level regulation of liquid and vapour conductances. Photosynthetic capacity also increased with Kleaf, however, it became saturated at values of Kleaf over 20 mmol m-2 s-1 MPa-1. * The data suggest that vessels in the leaves of the angiosperms studied provide them with the flexibility to produce highly conductive leaves with correspondingly high photosynthetic capacities relative to tracheid-bearing species.     

Phyllosphere nitrogen relations: reciprocal transfer of nitrogen between epiphyllous liverworts and host plants in the understorey of a lowland tropical wet forest in Costa Rica

Epiphyllous bryophytes on tropical rainforest plants acquire nutrients from throughfall and free-living N2-fixing organisms, but may also depend directly on host leaf leachates. By contrast, after drying events bryophytes lose significant quantities of nutrients through leaching that can be taken up by host leaves. To assess a potential nutritional interdependency, nitrogen fluxes between epiphyllous liverworts and their host leaves (Carludovica drudei, Costus laevis, Dieffenbachia concinna, Pentagonia wendlandii) were quantified by in situ15N-labelling techniques in a lowland rainforest, Piedras Blancas National Park, Costa Rica. Depending on host species, epiphyllous bryophytes met between 1 and 57% of their N demand from host leaf leachates. Externally supplied 15N was taken up both by epiphylls and host leaves, but N from epiphyll leachates accounted for < 2.5% of host leaf N after 14 d. Long-term observations (180 d) demonstrated the highly dynamic nature of phyllosphere N of the investigated tropical rainforest understorey and an intermittent sink capacity of epiphyllous bryophytes.     

Habitat Use of Juvenile Fish in the Lower Danube and the Danube Delta: Implications for Ecotone Connectivity

Functional processes in freshwater ecosystems are highly influenced by acidic conditions. Foodwebs are affected and macroinvertebrate species diversity is decreased. This study aims to investigate leaf decomposition at very low pH in the acidic Banyupahit–Banyuputih river originating from the acidic crater lake Kawah Ijen in Indonesia. Leaf decomposition experiments were carried out for 200 days in the acidic river at pHs of approximately 0.7, 2.3 and 3.0 and in the neutral Kali Sengon river, using leaves from teak, Tectona grandis, and bamboo, Bambusa sp. Two different types of leaf packs were used: fine mesh size packs were used to exclude macroinvertebrates and coarse mesh size packs allowed macroinvertebrate colonization. Clear differences in decomposition rate were observed between the neutral Kali Sengon and the acidic Banyupahit–Banyuputih river with decomposition in the Kali Sengon river proceeding significantly faster for both leaf types. In the Kali Sengon k values (d⁻¹) over 46 days were 0.0202 for fine teak, 0.0236 for coarse teak, 0.0114 for fine bamboo and 0.0151 for coarse bamboo. No significant differences were observed between the three sites in the acidic Banyupahit–Banyuputih river with k values of 0.0034–0.0066 for fine teak, 0.0002–0.0057 for coarse teak, 0.0029–0.0054 for fine bamboo and 0.0000–0.0068 for coarse bamboo. Moreover, no clear adaptation of macroinvertebrates or microbes to low pH conditions could be detected. The coarse mesh leaf packs in the neutral Kali Sengon river revealed that macroinvertebrates are important in the breakdown process. Fine mesh packs revealed that microbial activity is depressed under acidic conditions. Based on this evidence, we conclude that the toxicity at low pH conditions, and probably also the precipitation of metals on the leaf material, seriously affects leaf decomposition.     

Diffusion in plant cuticles as affected by temperature and size of organic solutes: similarity and diversity among species

Mobilities of lipophilic organic solutes in cuticular membranes (CM) isolated from mature leaves of Citrus aurantium L., Citrus grandis L., Hedera helix L., IIex aquifolium L., Ilex paraguariensis St.-Hil., Mains domestica Borkh., Prunus armeniaca L., Primus laurocerasus L., Pyrus communis L., Pyrus pyrifolia (Burm. f.) Nakai, Stephanotis florihunda Brongn. and Strophantus gratus Baill. were measured over a temperature range of 15–78°C. In this range, solute mobilities increased up to 1000-fold, which corresponds to temperature coefficients Q₁₀ of 3 (IAA in P. armeniaca) to 14 (cholesterol in H. helix). For most species, Arrhenius graphs showed good linearity up to 40°C, and up to 78°C for some species, while for others activation energies declined with increasing temperature. However, no distinct phase transitions caused by sudden structural changes in the CM were observed. In three species we examined whether heating to 70°C changed solute mobility irreversibly by comparing Arrhenius graphs for two successive experiments with the same CM. The two graphs were very similar for P. laurocerasus, while mobilities in the second graph were somewhat reduced for C. aurantium and greatly increased (at 25 and 35°C) for H. helix. This indicates rearrangements of at least some wax constituents when heated to high temperatures. The activation energies of diffusion (E_D) ranged from 75 to 189 KJ mol^?11 depending on species and solute size. Size selectivity and variability between cuticles decreased with increasing temperature, and this is caused by differences in (E_D). An excellent correlation between the pre-exponential factor of the Arrhenius equation and E_D was observed, which is evidence that organic solutes differing greatly in molecular size (130–349 cm³ mol^?1) and cuticle/water partition coefficient (25–10⁸) use similar diffusion paths in the CM of all 12 plant species tested. Diffusion occurs in regions with identical physicochemical properties and differs only in magnitude.     

Contractile roots in succulent monocots: convergence, divergence and adaptation to limited rainfall

Contractile roots (CRs) that pull shoots further down in the soil are a possible example of convergent evolution in two monocot families, the Agavaceae and the Asphodelaceae. The association between CRs, water uptake and habitat aridity was investigated for agaves, yuccas and aloes by assessing the occurrence of CRs and the amount of root contraction for glasshouse-grown plants with respect to mean annual rainfall of their native habitats. Structural features of CRs as well as root hydraulic conductance were compared with those of non-contractile roots (NCRs). CRs occurred in 55% of the 73 species examined, including 64% of the agaves and 85% of the yuccas, but in none of the aloes despite the occurrence of CRs in related genera. The phylogenetic distribution of CRs was consistent with multiple acquisitions or losses of the trait. The amount of root contraction showed a highly significant negative relationship with mean annual rainfall, although other environmental factors may also be important. Radial hydraulic conductance of the basal (contractile) zone exceeded that of the midroot zone for CRs; for NCRs, the opposite was true. Thus, CRs in the species examined may provide a mechanism for greater water uptake near the soil surface in regions with limited rainfall.     

Rapid response of the plasma-membrane potential in oat coleoptiles to auxin and other weak acids

We have compared the effects of the auxin, indole-3-acetic acid (IAA) with that of other weak acids on the plasma-membrane potential of oat (Avena sativa L.) coleoptile cells. Cells treated with 1 M IAA at pH 6 depolarize 20–25 mV in 10–12 min, but they then repolarize, until by 20–25 min their potentials are about 25 mV more negative than the initial value. Similar concentrations of benzoic and butyric acids cause the initial depolarization, but not the subsequent hyperpolarization. The hyperpolarization is therefore specific to IAA. All the weak acids, including IAA, evoke a rapid hyperpolarization when their concentrations are raised to 10 mM. This result indicates that at high concentrations, the uptake of undissociated weak acids activates electrogenic proton pumping, most likely by lowering cytoplasmic pH. In contrast, the hyperpolarization observed with concentrations of IAA four orders of magnitude lower appears to be a specific hormonal effect. This specific, auxin-induced hyperpolarization occurs at the same time as the initiation of net proton secretion and supports the hypothesis that auxin initiates extension growth by increasing proton pumping.Abbreviations FC fusicoccin - IAA indole-3-acetic acid     

Interspecies variation in nitrogen uptake kinetic responses of temperate forest species to elevated CO2: potential causes and consequences

Despite the recognition that the capacity to acquire N is critical in plant response to CO₂ enrichment, there is little information on how elevated CO₂ affects root N uptake kinetics. The few available data indicate a highly variable pattern of response to elevated CO₂, but it is presently unclear if the observed inconsistencies are caused by differences in experimental protocols or by true species differences. Furthermore, if there are interspecific variations in N uptake responses to elevated CO₂, it is not clear whether these are associated with different functional groups. Accordingly, we examined intact root‐system NH₄⁺ and NO₃^– uptake kinetic responses to elevated CO₂ in seedlings of six temperate forest tree species, representing (i) fast‐ vs. slow‐growers and (ii) broad‐leaves vs. conifers, that were cultured and assayed in otherwise similar conditions. In general, the species tested had a higher uptake capacity (V_max) for NH₄⁺ than for NO₃^–. Species substantially differed in their NO₃^– and NH₄⁺ uptake capacities, but the interspecific differences were markedly greater for NO₃^– than NH₄⁺ uptake. Elevated CO₂ had a species‐dependent effect on root uptake capacity for NH₄⁺ ranging from an increase of 215% in Acer negundo L. to a decrease of about 40% in Quercus macrocarpa Michx. In contrast, NO₃^– uptake capacity responded little to CO₂ in all the species except A. negundo in which it was significantly down‐regulated at elevated CO₂. Across species, the capacity for NH₄⁺ uptake was positively correlated with the relative growth rate (RGR) of species; however, the CO₂ effect on NH₄⁺ uptake capacity could not be explained by changes in RGR. The observed variation in NH₄⁺ uptake response to elevated CO₂ was also inconsistent with life‐form differences. Other possible mechanisms that may explain why elevated CO₂ elicits a species‐specific response in root N uptake kinetics are discussed. Despite the fact that the exact mechanism(s) for such interspecific variation remains unresolved, these differences may have a significant implication for competitive interactions and community responses to elevated CO₂ environment. We suggest that differential species responses in nutrient uptake capacity could be one potential mechanism for the CO₂‐induced shifts in net primary productivity and species composition that have been observed in experimental communities exposed to elevated levels of CO₂.