Decline of Leaf Hydraulic Conductance with Dehydration: Relationship to Leaf Size and Venation Architecture    

Abstract

Across plant species, leaves vary enormously in their size and their venation architecture, of which one major function is to replace water lost to transpiration. The leaf hydraulic conductance (K leaf ) represents the capacity of the transport system to deliver water, allowing stomata to remain open for photosynthesis. Previous studies showed that K leaf relates to vein density (vein length per area). Additionally, venation architecture determines the sensitivity of K leaf to damage; severing the midrib caused K leaf and gas exchange to decline, with lesser impacts in leaves with higher major vein density that provided more numerous water flow pathways around the damaged vein. Because xylem embolism during dehydration also reduces K leaf , we hypothesized that higher major vein density would also reduce hydraulic vulnerability. Smaller leaves, which generally have higher major vein density, would thus have lower hydraulic vulnerability. Tests using simulations with a spatially explicit model confirmed that smaller leaves with higher major vein density were more tolerant of major vein embolism. Additionally, for 10 species ranging strongly in drought tolerance, hydraulic vulnerability, determined as the leaf water potential at 50% and 80% loss of K leaf , was lower with greater major vein density and smaller leaf size (|r| = 0.85-0.90; P , 0.01). These relationships were independent of other aspects of physiological and morphological drought tolerance. These findings point to a new functional role of venation architecture and small leaf size in drought tolerance, potentially contributing to well-known biogeographic trends in leaf size.

Developmentally based scaling of leaf venation architecture explains global ecological patterns

“…However, despite the strong potential importance of such trends, there have not been any previous conclusive tests for the scaling of vein traits with leaf size across species. Data from three previous studies with ten or fewer species showed a negative scaling of major vein density with leaf size, and minor vein density was independent of leaf size 8,12,13 . A further study using automated analyses of low-resolution images reported vein density to be independent of leaf size across 339 species 14 ; however, that study measured only a fraction of the vein system and did not distinguish among vein orders 14 and thus, did not allow a conclusive test of general scaling of vein traits.…”

“…However, the scaling of major vein density provides a direct, hydraulically based mechanism. Modelling and experiments showed that such higher major vein density in smaller leaves in principle provides redundant 'superhighways' for water transport that contribute to drought tolerance by routing water around blockages caused by drought-induced xylem embolism, and additionally protect the hydraulic system from vein damage 8,13 .…”

“…Notably, the dicotyledon developmental programme allows for not only large, competitive leaves, but a dramatic range of leaf sizes with a wide spectrum of total vein densities and photosynthetic rates 16 . For example, a large leaf may be selected for a plant of a moist area, for effective light capture and photosynthesis relative to biomass allocation 44 , and a small leaf may be selected in drought-tolerant species 8 ; both may have high minor vein densities, enabling high photosynthetic rates when water is available. The potential of angiosperms to vary strongly in vein density enables dominance in a far greater range of habitats than other plant lineages 3,6,48 , especially as leaf size can adapt independently to optimise other ecological benefits against costs 6,7,44 .…”

“…Across species, leaf venation shows enormous structural diversity, the more remarkable because of its shared development and functions. The functional consequences of leaf venation have attracted increasing interest in a widening range of fields, because vein traits, including vein diameters and densities ( = length per leaf area), as well as leaf size are key determinants of plant performance and indeed of shifts in the lineages that dominated the world vegetation through deep time [1][2][3][4][5][6][7][8][9] .…”

Weak coordination among petiole, leaf, vein, and gas‐exchange traits across Australian angiosperm species and its possible implications

“…Furthermore, we might also expect species exhibiting marked resistance to hydraulic dysfunction to exhibit greater redundancy (Scoffoni et al. 2011), and therefore, poor coordination between liquid‐ and gas‐phase conductive capacities.…”