Maximum leaf conductance driven by CO₂ effects on stomatal size and density over geologic time

Stomatal pores are microscopic structures on the epidermis of leaves formed by 2 specialized guard cells that control the exchange of water vapor and CO₂ between plants and the atmosphere. Stomatal size (S) and density (D) determine maximum leaf diffusive (stomatal) conductance of CO₂ (gcmax) to sites of assimilation. Although large variations in D observed in the fossil record have been correlated with atmospheric CO₂, the crucial significance of similarly large variations in S has been overlooked. Here, we use physical diffusion theory to explain why large changes in S necessarily accompanied the changes in D and atmospheric CO₂ over the last 400 million years. In particular, we show that high densities of small stomata are the only way to attain the highest gcmax values required to counter CO₂"starvation" at low atmospheric CO₂ concentrations. This explains cycles of increasing D and decreasing S evident in the fossil history of stomata under the CO₂ impoverished atmospheres of the Permo-Carboniferous and Cenozoic glaciations. The pattern was reversed under rising atmospheric CO₂ regimes. Selection for small S was crucial for attaining high gcmax under falling atmospheric CO₂ and, therefore, may represent a mechanism linking CO₂ and the increasing gas-exchange capacity of land plants over geologic time.