Hydraulic adjustments alter limits on transpiration at glacial vs. current and future predicted atmospheric [CO2]

Background/Question/Methods

Since the last glacial maximum, atmospheric carbon dioxide concentration [CO₂] has more than doubled, and is predicted to double yet again in the coming century. Across this entire range of [CO₂] trade-offs between water use and carbon gain can limit productivity, but the strength of this limitation may become weaker as [CO₂] increases. Hydraulic limits on water use are set by plant and soil hydraulic characters which determine the maximum transpiration rate (E_crit), beyond which hydraulic failure results in plant death. In the absence of drought, when plant water potential (Ψ) is high, plants often maintain transpiration well below E_crit, as other factors arise to limit carbon gain. As Ψ declines during drought, however, E_crit also declines, necessitating reduced transpiration. A positive relationship between [CO₂] and Ψ suggests that plants grown at glacial [CO₂] may closely approach E_crit, particularly during drought, placing them at high risk of hydraulic failure. As [CO₂] increases and other factors begin to limit carbon gain, plants may maintain transpiration far below E_crit, reducing the risk of hydraulic failure. Alternatively, plants could maintain a similar risk of hydraulic failure across a range of [CO₂] by adjusting hydraulic characters which determine E_crit. To address these competing hypotheses we grew the annual Phaseolus vulgaris at glacial (180 ppm), current (380 ppm) and future predicted (700 ppm) [CO₂], under four drought regimes, from well-watered to severe drought stress. We estimated E_crit using a transport model (Sperry et al. 1998) parameterized with data on xylem hydraulic structure and function, gas exchange and biomass allocation.

Results/Conclusions

The risk of hydraulic failure did not diminish as [CO₂] increased, rather E_crit declined with increasing [CO₂]. Differences in E_crit resulted from adjustment of plant hydraulic characters: there was a negative relationship between leaf specific xylem hydraulic conductance and [CO₂], and plants grown at glacial [CO₂] exhibited lower percent loss of hydraulic conductance in response to drought than plants grown at either current or future [CO₂]. This functional difference was reflected in xylem structure, and we observed a negative relationship between vessel implosion strength and [CO₂]. These results suggest that during glacial periods plants were able to improve carbon gain through structural and functional plasticity which altered hydraulic limits on transpiration. Though plants grown a future predicted [CO₂] will likely exhibit reduced transpiration, our study suggests they will be more susceptible to drought-induced hydraulic failure than those grown under glacial or current [CO₂] conditions.