Theoretical analyses reveal how plant investment in the architecture of leaf veins can be shuffled for different conditions, minimizing the construction costs associated with supplying water to leaves.
In the very first chapter of his magnificent 1727 book Vegetable Staticks, the pioneering English plant physiologist Stephen Hales observed1 that plants lose water by “perspiration”. He then went one better by conducting experiments to quantify the process. Today, through what we now know as Earth's 'transpiration engine', terrestrial plants add 32 × 103 billion tonnes of water vapour to the atmosphere annually — equivalent to about 30% of the precipitation that falls on land and double the total amount of water vapour in the atmosphere2. This huge global flux of water vapour passes through microscopic stomatal pores on the surface of leaves and represents a fundamental ecosystem service, contributing to the global water cycle and climate regulation by cloud formation. Writing in The American Naturalist, McKown et al.3 provide a thought-provoking theoretical analysis that reveals how plants configure the internal pipe network (vasculature) of leaves to deliver more water for a given carbon investment in these specialized tissues.
The flowering plants (angiosperms) that dominate the tropical rainforests experience uniform year-round warmth and high irradiance, and with their sophisticated leaf vascular architecture have the greatest rates of transpiration on Earth2. To maintain such high rates of water loss, angiosperms have a relatively high density of veins (total vein length per unit leaf area) forming the pipe network that carries water from the leaf stem to the photosynthesizing tissues. This effectively brings the water source and the evaporating sites within the leaf closer together to improve the leaf's overall hydraulic conductance. But a consequence, McKown et al.3 show, is higher leaf-construction costs because it requires additional specialized water-conducting tissues rich in carbon-costly lignin.
Until now, these hidden carbon costs have tended to be overlooked, but McKown and colleagues' analysis reveals the strategies employed by angiosperms to help minimize them. The findings are particularly illuminating in an evolutionary context. A feature in the evolution of angiosperm leaves, and one that marks the final emergence of the terrestrial biosphere's transpiration engine, is the apparent surge in the density of veins during the angiosperms' rise to global dominance from the early Cretaceous (130 million years ago) onwards4 that took place against a backdrop of falling atmospheric carbon dioxide concentrations5 (Fig. 1a, overleaf). When considered alongside the findings of McKown et al., this observation raises the question as to why evolution apparently drove the selection of leaves with a capacity for higher transpiration rates despite a rising carbon penalty for construction.
The answer emerges with the realization that the processes of transpiration and CO2 uptake for photosynthesis are tightly coupled. Under recent relatively low CO2 concentrations, leaves capable of fast rates of photosynthesis require large numbers of small stomatal pores, which creates a high stomatal conductance to CO2 but inevitably permits the escape of more water as transpiration. The whole process proceeds providing plants maintain the hydraulic pathway of water from the soil to leaves.
Now consider the situation early in the Cretaceous, when a CO2-rich atmosphere fertilized photosynthesis in leaves constructed with fewer stomatal pores and lower transpiration rates. In these circumstances, a modestly engineered leaf vascular system, with low vein density, was perfectly adequate. The long, slow decline in the concentration of atmospheric CO2 over the next 130 million years forced plants to increase leaf stomatal conductance to CO2 (Fig. 1), leading to higher rates of transpirational water loss6. Plants supported this additional water loss with improved vascular systems that could outcompete their predecessors, effectively a 'hydraulic arms race' amongst species (Fig. 1b). This CO2-driven selection of leaves with a greater capacity to exchange gases with the atmosphere had to be coordinated with greater hydraulic flow, as provided by additional vein infrastructure but with a steadily increasing construction cost — particularly when expressed relative to photosynthetic rates (Fig. 1, vein density/photosynthesis rate). Relative construction costs escalated dramatically over the past 50 million years, as photosynthetic rates declined with falling CO2.
McKown et al.3 show that the angiosperm solution to this evolutionary problem involved more than greater vein density. Like reticulated water supplies to towns, leaf veins are configured in a hierarchical order, branching from larger, 'low-order' conduits to ever smaller, 'higher-order' conduits. Depending on how a plant shuffles its investment into these different vein categories, the cost of increased hydraulic conductance can vary enormously. Theoretically, increasing the density of the highest-order, or 'minor veins', together with vein tapering, is by far the most cost-effective strategy3, and indeed both were evolutionary innovations in angiosperms. These innovations allowed higher leaf hydraulic conductances and faster rates of photosynthesis for a given carbon investment in lignified tissues.
Theoretical cost–benefit models such as that used by McKown et al.3 are valuable, but are still in their infancy. They require improvement to facilitate rigorous evaluation against observations, and representation of a broader range of transpiration functions7. Vascular tissues of leaves and stems, for example, provide mechanical support and, because they are lignin-rich, they contain less nitrogen and phosphorus than actively photosynthesizing tissues. Modification of the ecological stoichiometry of nutrient use during photosynthesis and transpiration7 is, then, one possible consequence of the Cretaceous evolution of angiosperms that have higher vein densities.
For all his pioneering studies on plant–water relations, Hales didn't discover that plants transpire water from leaves or that this flux of water is regulated by stomatal pores studding the epidermis. Inspired by Isaac Newton and Robert Boyle to bring precision to his “natural philosophizing”, he did calculate the burden of “perspiration” to plants as they grow1. But the hidden additional costs and functions of this process are only now being unveiled.
Ayres, P. The Aliveness of Plants: The Darwins at the Dawn of Plant Science (Pickering & Chatto, 2008).
Hetherington, A. M. & Woodward, F. I. Nature 424, 901–908 (2003).
McKown, A. D., Cochard, H. & Sack, L. Am. Nat. 175, 447–460 (2010).
Brodribb, T. J. & Feild, T. S. Ecol. Lett. 13, 175–183 (2010).
Fletcher, B. J., Brentnall, S. J., Anderson, C. W., Berner, R. A. & Beerling, D. J. Nature Geosci. 1, 43–48 (2008).
Franks, P. J. & Beerling, D. J. Geobiology 7, 227–236 (2009).
Raven, J. A. New Phytol. 179, 905–907 (2008).
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