Height-associated variation in leaf anatomy of tall redwoods: potential impacts on whole-tree carbon balance

The tallest tree species, coast redwood (Sequoia sempervirens), provides an ideal model for investigating both the adaptations allowing maximum height growth in plants and the factors that limit it. Within the crowns of tall redwoods there exists broad variation in leaf anatomy, much of which is better explained by height-induced hydraulic constraints than by differences in light environment. We analyzed the anatomy of leaves and stems collected at 10-m intervals from both the inner and outer crowns in five redwoods 108 to 113 m tall. Mesophyll porosity, a factor known to limit leaf carbon fixation rates, strongly decreased with height. Leaf width also decreased with height while thickness increased, such that leaf cross-sectional area remained constant but the surface area to volume ratio was minimized at the treetop, again indicative of reduced gas exchange capacity per unit tissue volume. Likewise, height-associated decreases in leaf length and xylem cross-sectional area were accompanied by increased investment in transfusion tissue, and thus a whole-leaf vascular volume that did not significantly change with height in most trees. Transfusion tracheids became increasingly deformed with height, which suggests that they may be collapsing under the extreme water stress of the upper crown and thus acting as a hydraulic buffer that mitigates leaf water stress and reduces the likelihood of xylem dysfunction. Functional traits such as investment in leaf thickness and transfusion tissue may serve to improve desiccation tolerance where it is needed most, but at a presumably high carbon cost. Anatomical changes resulting from reduced leaf expansion correspond to the previously documented increase in leaf mass/area ratio and decreases in photosynthetic capacity and internal gas-phase conductance in redwood. Thus, height-induced hydraulic stress appears to drive a gradient in leaf anatomy that may override most among-tree developmental variation and have a profound effect on whole-tree carbon balance as maximum height is approached in Earth's tallest plants.