Are diurnal stomatal dynamics governed by Cowan-Farquhar optimality principles?

Despite the critical role of stomata in regulating plant water use (transpiration) and carbon uptake (assimilation) during diurnal fluctuations, current land surface models rely on plant functional type-specific parameterization of stomatal conductance (g_sw) that often struggles to reproduce observed stomatal dynamics. In particular, most established models ignore potential feedback between stomatal conductance and the within-canopy air space: an increase in g_sw humidifies and cools the air surrounding the leaf, and decreases the vapor pressure deficit of the leaf (VPD_leaf), which can further increase g_sw. This creates a positive feedback loop that complicates distinguishing whether stomatal dynamics are a simple response to environmental variations (e.g. VPD_air or light intensity) or a result of stomatal optimization in the presence of leaf-air feedback. A thorough understanding of these processes is crucial for modeling water and carbon fluxes under changing environmental conditions.

We measured continuous in situ gas exchange from individual leaves of wheat (Triticum aestivum) during multiple diurnal cycles under natural fluctuations of VPD_leaf and light intensity driven by cloud cover. By adjusting chamber air exchange rate, we manipulated the strength of the experimental leaf-airfeedback, given that a low exchange rate makes the air inside the measurement cuvette more sensitive to leaf heat and gas exchange. Diurnal variations in g_sw spanned an order of magnitude multiple times during the day, demonstrating the responsiveness of g_sw to fluctuating environmental conditions and feedback strengths.

The stomatal optimality principle of Cowan and Farquhar (1977) predicts that g_sw adjusts dynamically to environmental conditions to maximize the time-integral of carbon gain under constrained water availability by maintaining a constant marginal water cost (∂E) per carbon uptake (∂A) (λ = ∂E/∂A). According to the theory, the operational slope λ is constant among leaves of the same plant and responds only to soil moisture (θ). By measuring E and A simultaneously and calculating λ at stable light conditions (≥ 5 min), we test, in both laboratory and field studies, whether the operational slope λ converges to a similar value among leaves of the same plants, remains constant throughout a day and declines with reduced θ.

If λ proves to be stable between leaves of the same plant while responding to θ, an empirical relation between λ and θ within the root zone could serve as a powerful trait for predicting stomatal dynamics in wheat plants. It remains to be assessed how λ(θ), and therefore optimality principles, vary among cultivars and generations, whether it is equally useful for other species, and whether it is conserved under environmental change. The new method of measuring leaf-scale λ presented here opens the path to such studies.