Optimal balancing of xylem efficiency and safety explains plant vulnerability to drought

Abstract

In vast areas of the world, forests and vegetation are water limited and plant survival depends on the ability to avoid catastrophic hydraulic failure. Therefore, it is remarkable that plants take hydraulic risks by operating at water potentials (ψ) that induce partial failure of the water conduits (xylem). Here we present an eco-evolutionary optimality principle for xylem conduit design that explains this phenomenon based on the hypothesis that conductive efficiency and safety are optimally co-adapted to the environment. The model explains the relationship between the tolerance to negative water potential (ψ₅₀ ) and the environmentally dependent minimum ψ (ψ_min ) across a large number of species, and along the xylem pathway within individuals of two species studied. The wider hydraulic safety margin in gymnosperms compared to angiosperms can be explained as an adaptation to a higher susceptibility to accumulation of embolism. The model provides a novel optimality-based perspective on the relationship between xylem safety and efficiency.

Keywords: conductivity; embolism; functional traits; optimality; tracheids; trees; vessels; vulnerability; xylem.