Scaling between stomatal size and density in forest plants

The size and density of stomatal pores limit the maximum rate of leaf carbon gain and water loss (gmax) in land plants. Stomatal size and density are negatively correlated at broad phylogenetic scales, such that species with small stomata tend to have greater stomatal density, but the consequences of this relationship for leaf function have been controversial. The prevailing hypothesis posits that the negative scaling of size and density arises because species that evolved higher gmax also achieved reduced allocation of epidermal area to stomata (stomatal-area minimization). Alternatively, the negative scaling of size and density might reflect the maintenance of a stable mean and variance in gmax despite variation in stomatal size and density, which would result in a higher allocation of epidermal area to achieve high gmax (stomatal-area increase). Here, we tested these hypotheses by comparing their predictions for the structure of the covariance of stomatal size and density across species, applying macroevolutionary models and phylogenetic regression to data for 2408 species of angiosperms, gymnosperms, and ferns from forests worldwide. The observed stomatal size-density scaling and covariance supported the stomatal-area increase hypothesis for high gmax. Thus, contrary to the prevailing view, higher gmax is not achieved while minimizing stomatal area allocation but requires increasing epidermal area allocated to stomata. Understanding of optimal stomatal conductance, photosynthesis, and plant water-use efficiency used in Earth System and crop productivity models will thus be improved by including the cost of higher gmax both in construction cost of stomata and opportunity cost in epidermal space.