A dynamic leaf gas‐exchange strategy is conserved in woody plants under changing ambient CO₂: evidence from carbon isotope discrimination in paleo and CO₂ enrichment studies

Abstract

Rising atmospheric [CO2 ], ca , is expected to affect stomatal regulation of leaf gas-exchange of woody plants, thus influencing energy fluxes as well as carbon (C), water, and nutrient cycling of forests. Researchers have proposed various strategies for stomatal regulation of leaf gas-exchange that include maintaining a constant leaf internal [CO2 ], ci , a constant drawdown in CO2 (ca - ci ), and a constant ci /ca . These strategies can result in drastically different consequences for leaf gas-exchange. The accuracy of Earth systems models depends in part on assumptions about generalizable patterns in leaf gas-exchange responses to varying ca . The concept of optimal stomatal behavior, exemplified by woody plants shifting along a continuum of these strategies, provides a unifying framework for understanding leaf gas-exchange responses to ca . To assess leaf gas-exchange regulation strategies, we analyzed patterns in ci inferred from studies reporting C stable isotope ratios (δ(13) C) or photosynthetic discrimination (∆) in woody angiosperms and gymnosperms that grew across a range of ca spanning at least 100 ppm. Our results suggest that much of the ca -induced changes in ci /ca occurred across ca spanning 200 to 400 ppm. These patterns imply that ca - ci will eventually approach a constant level at high ca because assimilation rates will reach a maximum and stomatal conductance of each species should be constrained to some minimum level. These analyses are not consistent with canalization toward any single strategy, particularly maintaining a constant ci . Rather, the results are consistent with the existence of a broadly conserved pattern of stomatal optimization in woody angiosperms and gymnosperms. This results in trees being profligate water users at low ca , when additional water loss is small for each unit of C gain, and increasingly water-conservative at high ca , when photosystems are saturated and water loss is large for each unit C gain.

20th century changes in carbon isotopes and water-use efficiency: tree-ring-based evaluation of the CLM4.5 and LPX-Bern models

“…As reported by Voelker et al (2016), studies that are consistent with the notion of constant c i /c a include early work by Wong et al (1979) measuring A and g of leaves in a chamber, and a range of tree-ring δ 13 C studies (Saurer et al, 2004;Ward et al, 2005;Bonal et al, 2011;Franks et al, 2013), as well as a metaanalysis of FACE experiments (Ainsworth and Long, 2005). The European δ 13 C tree-ring records analyzed by Frank et al (2015) and Saurer et al (2014) also point to a moderate control towards a constant c i /c a ratio.…”

“…Out of 35 studies with growth data, 18 show an increase in growth with time, while the others show no growth changes or negative growth changes. Voelker et al (2016) analyzed studies of δ 13 C and photosynthetic discrimination in woody angiosperms and gymnosperms that grew across a range of CO 2 spanning at least 100 ppm and combining paleodata, tree-ring records, and FACE-type experiments. They conclude that woody plants respond to increasing CO 2 by regulating leaf gas exchange along a continuum of c a − c i and c i /c a that minimizes water loss for a given amount of C gain and therefore increasingly minimizes the likelihood of exposure to drought stress.…”

“…There is a rich body of literature on changes in 13 C isotopic discrimination and iWUE and on observational evidence from δ 13 C tree-ring records McCarroll and Loader, 2004;Fichtler et al, 2010;Leonardi et al, 2012;Churakova , Sidorova, S;Lévesque et al, 2014;Liu et al, 2014b;Saurer et al, 2014;Hartl-Meier et al, 2015;Voelker et al, 2016), free-air CO 2 enrichment (FACE)-type experiments (Battipaglia et al, 2013;Klein et al, 2016), δ 13 C site measurements (Pataki et al, 2003;Bowling et al, 2014), and δ 13 C paleodata (Voelker et al, 2016). These data generally suggest small to moderate decadal-to-century-scale changes in discrimination that correspond to a 20th century increase in iWUE On the order of 20 % and physiological control towards a constant ratio of the partial pressure of CO 2 within the leaf's substomatal cavities to the CO 2 pressure outside the leaf (c i /c a ; Saurer et al, 2004;Leonardi et al, 2012;Frank et al, 2015) and, more generally, a pattern of stomatal optimization towards minimizing water loss per unit carbon assimilated (Voelker et al, 2016).…”

“…These data generally suggest small to moderate decadal-to-century-scale changes in discrimination that correspond to a 20th century increase in iWUE On the order of 20 % and physiological control towards a constant ratio of the partial pressure of CO 2 within the leaf's substomatal cavities to the CO 2 pressure outside the leaf (c i /c a ; Saurer et al, 2004;Leonardi et al, 2012;Frank et al, 2015) and, more generally, a pattern of stomatal optimization towards minimizing water loss per unit carbon assimilated (Voelker et al, 2016). The δ 13 C data are used to evaluate global and local models of plant growth, carbon cycling, and land-atmosphere isotopic fluxes for atmospheric carbon balancing (Scholze et al, 2003(Scholze et al, , 2008Suits et al, 2005;Danis et al, 2012;van der Velde et al, 2014).…”

Carbon isotope discrimination in C3 land plants is independent of natural variations in pCO2

“…At present, the most discrepant study (Schubert and Jahren, 2012) represents short-term experiments on two forbs (Arabidopsis and radish). As discussed recently (Diefendorf et al, 2015;Voelker et al, 2015), plants may exhibit short-term phenotypic and isotopic changes in response to abrupt changes to p CO2 , but on evolutionary timescales (decades to centuries) may evolve towards an optimal physiology whose isotopic fractionation is p CO2 -independent. Short-term experiments might have relevance for modern rapid changes to p CO2 , but not for ancient isotope records.…”