Restricted internal diffusion weakens transpiration-photosynthesis coupling during heatwaves: Evidence from leaf carbonyl sulphide exchange

Abstract

Increasingly frequent and intense heatwaves threaten ecosystem health in a warming climate. However, plant responses to heatwaves are poorly understood. A key uncertainty concerns the intensification of transpiration when heatwaves suppress photosynthesis, known as transpiration-photosynthesis decoupling. Field observations of such decoupling are scarce, and the underlying physiological mechanisms remain elusive. Here, we use carbonyl sulphide (COS) as a leaf gas exchange tracer to examine potential mechanisms leading to transpiration-photosynthesis decoupling on a coast live oak in a southern California woodland in spring 2013. We found that heatwaves suppressed both photosynthesis and leaf COS uptake but increased transpiration or sustained it at non-heatwave levels throughout the day. Despite statistically significant decoupling between transpiration and photosynthesis, stomatal sensitivity to environmental factors did not change during heatwaves. Instead, midday photosynthesis during heatwaves was restricted by internal diffusion, as indicated by the lower internal conductance to COS. Thus, increased evaporative demand and nonstomatal limitation to photosynthesis act jointly to decouple transpiration from photosynthesis without altering stomatal sensitivity. Decoupling offered limited potential cooling benefits, questioning its effectiveness for leaf thermoregulation in xeric ecosystems. We suggest that adding COS to leaf and ecosystem flux measurements helps elucidate diverse physiological mechanisms underlying transpiration-photosynthesis decoupling.

Keywords: COS:CO2 leaf relative uptake (LRU); Mediterranean ecosystems; carbonyl sulphide (COS or OCS); coast live oak (Quercus agrifolia); heatwaves; nonstomatal limitation; stomatal responses; transpiration–photosynthesis coupling.