Leaf palmate venation and vascular redundancy confer tolerance of hydraulic disruption

Abstract

Leaf venation is a showcase of plant diversity, ranging from the grid-like network in grasses, to a wide variety of dendritic systems in other angiosperms. A principal function of the venation is to deliver water; however, a hydraulic significance has never been demonstrated for contrasting major venation architectures, including the most basic dichotomy, "pinnate" and "palmate" systems. We hypothesized that vascular redundancy confers tolerance of vein breakage such as would occur during mechanical or insect damage. We subjected leaves of woody angiosperms of contrasting venation architecture to severing treatments in vivo, and, after wounds healed, made detailed measurements of physiological performance relative to control leaves. When the midrib was severed near the leaf base, the pinnately veined leaves declined strongly in leaf hydraulic conductance, stomatal conductance, and photosynthetic rate, whereas palmately veined leaves were minimally affected. Across all of the species examined, a higher density of primary veins predicted tolerance of midrib damage. This benefit for palmate venation is consistent with its repeated evolution and its biogeographic and habitat distribution. All leaves tested showed complete tolerance of damage to second- and higher-order veins, demonstrating that the parallel flow paths provided by the redundant, reticulate minor vein network protect the leaf from the impact of hydraulic disruption. These findings point to a hydraulic explanation for the diversification of low-order vein architecture and the commonness of reticulate, hierarchical leaf venation. These structures suggest roles for both economic constraints and risk tolerance in shaping leaf morphology during 130 million years of flowering plant evolution. © 2008 by The National Academy of Sciences of the USA.