Pushing the limits of C3 intrinsic water use efficiency in Mediterranean semiarid steppes: Responses of a drought-avoider perennial grass to climate aridification

© 2024 The Authors. Functional Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

1. Intrinsic water use efficiency (WUEi) reflects the trade-off between photosynthetic carbon gain and water loss through stomatal conductance and is key for understanding dryland plant responses to climate change. Stipa tenacissima is a perennial tussock C3 grass with an opportunistic, drought-avoiding water use strategy that dominates arid and semiarid steppes across the western Mediterranean region. However, its ecophysiological responses to aridification and woody shrub encroachment, a major land-use change in drylands worldwide, are not well-understood.

2. We investigated the variations in leaf stable isotopes (δ18O, δ13C, δ15N), nutrient concentrations (N, P, K), and culm water content and isotopic composition (δ18O, δ2H) of paired pure-grass and shrub-encroached S. tenacissima steppes along a 350 km aridity gradient in Spain (10 sites, 160 individuals).

3. Culm water isotopes revealed that S. tenacissima is a shallow-rooted grass that depends heavily on recent rainwater for water uptake, which may render it vulnerable to increasingly irregular rainfall combined with faster topsoil drying under climate warming and aridification. With increasing aridity, S. tenacissima enhanced leaf-level WUEi through more stringent stomatal regulation of plant water flux and carbon assimilation (higher δ13C and δ18O), reaching exceptionally high δ13C values (−23‰ to −21‰) at the most arid steppes. Foliar N concentration was remarkably low across sites regardless of woody shrub encroachment, evidencing severe water and N co-limitation of photosynthesis and productivity. Shrub encroachment decreased leaf P and K but did not affect S. tenacissima water status. Perennial grass cover decreased markedly with both declining winter rainfall and shrub encroachment suggesting population-level rather than individual-level responses of S. tenacissima to these changes.

4. The fundamental physiological constraints of photosynthetic C3 metabolism combined with low foliar N content may hamper the ability of S. tenacissima and other drought-avoider species with shallow roots to achieve further adaptive improvements in WUEi under increasing climatic stress. A drought-avoiding water use strategy based on early stomatal closure and photosynthesis suppression during prolonged rainless periods may thus compromise the capacity of semiarid S. tenacissima steppes to maintain perennial grass cover, sustain productivity and cope with ongoing climate aridification at the drier parts of their current distribution.

This research was funded and supported by grants from the Spanish Ministry of Science and Innovation (AGL-2006-11234; CGL2010-21064; CGL2013-48753-R; PID2019-107382RB-I00; PRX19/00301) awarded to JIQ, and grants by Fundación BBVA (BIOCON06/105) and Universidad Rey Juan Carlos (URJC-RNT-063-2) awarded to FTM. FTM also acknowledges support from the European Research Council (ERC Grant agreement 647038 [BIODESERT]), Generalitat Valenciana (CIDEGENT/2018/041) and the Spanish Ministry of Science and Innovation (EUR2022-134048). WR acknowledges partial support from the National Natural Science Foundation of China (41801091) and China Postdoctoral Science Foundation (2019T120868 and 2018M643542). SS was supported by a Ramón y Cajal fellowship (RYC-2016-20604) and the FOBIASS project (RTI2018-098895-A-100), both from the Spanish Ministry of Science and Innovation. PGP was supported by the DUALSOM project (PID2020-113021RA-I00) from the Spanish Ministry of Science and Innovation. IP was supported by the Fundación Séneca (project 20654/JLI/18). The authors thank María José Espinosa for help with laboratory work.

Peer reviewed