Are whole canopies optimized for carbon gain? How wasteful water use in shade leaves of Eucalyptus trees constrain theoretical relationships of photosynthesis and resource distribution
It is commonly assumed that stomatal conductance (gs) is optimised to maximise photosynthesis (A) while minimizing water loss, which has been confirmed for individual leaves under various manipulations of environmental drivers. When optimized, gs should be proportional to A along canopy light gradients, and thus the intercellular CO2 concentration (Ci) should not differ between sun and shade leaves (provided vapour pressure deficit is constant). Evidence from leaf C isotope discrimination (δ13C), however, generally indicates a lower Ci in sun leaves. Few datasets have compared Ci estimated from leaf gas exchange between sun and shade leaves, which is a more direct measure of stomatal behaviour. Although δ13C is used to infer Ci and water use efficiency, it actually represents the CO2 concentration inside the chloroplast (Cc), and the draw-down between Ci and Cc depends on mesophyll conductance (gm), and A. If gm is unaccounted for then relationships of stomatal control of A derived from δ13C along canopy gradients may be flawed. Here we investigate differences in stomatal behaviour between sun and shade leaves in Eucalyptus tereticornis trees grown in climate-controlled whole-tree chambers. We tested the optimization theory hypothesis that Ci is not different between sun and shade leaves when accounting for potential differences in gm. We studied the relationship between Ci and leaf nitrogen canopy distribution – a proxy for photosynthetic capacity, and hydraulic conductance (K) – a measure of water supply capacity. Additionally, gm was measured with online δ13Cmeasurements, using a tunable diode laser.
We found that A was reduced by ca. 40% in shade leaves associated with a 75% reduction in photosynthetically active radiation. Increases in A were proportional to gs in sun leaves, but this relationship was uncoupled in shade leaves. Photosynthetic capacity was lower in shade leaves (ca. 20% lower Vcmax and Jmax), but K did not differ. Leaf Ci, estimated from both δ13C and gas exchange, was lower in sun leaves. We reject the hypothesis that Ci is optimized throughout the canopy because shade leaves used more water with lower rates of A, as compared to sun leaves. This study provides evidence that theoretical relationships between A and optimal resource distribution may not hold true for all leaves within a canopy, and has consequences for models that scale A to the canopy.