Leaf anatomical traits determine the ¹⁸O enrichment of leaf water in coastal halophytes

Abstract

Anatomical adaptations to high-salinity environments in mangrove leaves may be recorded in leaf water isotopes. Recent studies observed lower O enrichment (Δ ) of leaf water with respect to source water in three mangrove species relative to adjacent freshwater trees, but the factors that govern this phenomenon remain unclear. To resolve this issue, we investigated leaf traits and Δ in 15 species of true mangrove plants, 14 species of adjacent freshwater trees, and 4 species of semi-mangrove plants at five study sites along south-eastern coast of China. Our results confirm that Δ was generally 3-4‰ lower for mangrove species than for adjacent freshwater or semi-mangrove species. We hypothesized that higher leaf water content (LWC) and lower leaf stomatal density (LS) both played important roles in reducing Δ in mangroves relative to nearby freshwater plants. Both differences acted to elongate effective leaf mixing length (L) in mangroves by about 200% and lower stomatal conductance by about 30%. Péclet models based on both LWC and LS could accurately predict Δ . Our findings highlight the potential species-specific anatomical determinants of Δ (or L), which has important implications for the interpretation of environmental information from metabolites produced by leaf water isotopes in palaeoclimate research.

The 18O‐signal transfer from water vapour to leaf water and assimilates varies among plant species and growth forms

“…About 50% of the MRT LW variation among plant species and growth forms was explained by metrics of leaf water content such as leaf succulence ( L S ) and leaf thickness ( L Th ; Figures c,d). This fits well with evidence that leaf water content affects the isotopic leaf water enrichment (Cernusak et al, ; Ellsworth, Ellsworth, Anderson, & Sternberg, ; Liang et al, ) and the δ 18 O of transpired water (Dubbert et al, ; Simonin et al, ; Song, Simonin, Loucos, & Barbour, ). High leaf water content likely causes a stronger dilution of the 18 O label, explaining the increase in MRT LW with L S .…”

“…High leaf water content likely causes a stronger dilution of the 18 O label, explaining the increase in MRT LW with L S . Given the influence of leaf water content on MRT LW and thus on steadystate conditions between water vapour and leaf water, nonlinear steady-state models (Song et al, 2015) should probably be used in studies including succulent species (Cernusak et al, 2008;Liang et al, 2018). In comparison, traits such as stomatal density and size were only weakly related to changes in MRT LW (Figures 4a,b vapour or condensed water on leaf surfaces (Goldsmith, 2013;Gotsch et al, 2014), a passive foliar water uptake along a potential leaf water gradient is unlikely given that plants were well watered.…”

“…A shorter MRT indicates a faster 18 O‐signal transfer, which is consistent with changes in the pool size and in the flux going through that pool (or both; Epron et al, ). Therefore, MRT values likely depend on leaf anatomical and morphological properties that can widely differ among plant growth forms (Cernusak, Mejia‐Chang, Winter, & Griffiths, ; Lai et al, ; Liang et al, ). Stomata are the primary entry point for δ 18 O V and thus differences in stomata pore size and density may influence the uptake of the atmospheric signal into the leaf water pool (Berry, Emery, Gotsch, & Goldsmith, ).…”

“…Thus, δ 18 O V variation is particularly important under high humidity conditions. Such conditions are often found in tropical and subtropical forests, where~50% of days can be very humid (>0.1 mm precipitation), closely followed by temperate and boreal forests (Dawson & Goldsmith, 2018 (Cernusak, Mejia-Chang, Winter, & Griffiths, 2008;Lai et al, 2008;Liang et al, 2018). Stomata are the primary entry point for δ 18 O V and thus differences in stomata pore size and density may influence the uptake of the atmospheric signal into the leaf water pool (Berry, Emery, Gotsch, & Goldsmith, 2018).…”

“…Stomata are the primary entry point for δ 18 O V and thus differences in stomata pore size and density may influence the uptake of the atmospheric signal into the leaf water pool (Berry, Emery, Gotsch, & Goldsmith, 2018). In addition, photosynthetic modes (PM; i.e., C 3 , C 4 , and crassulacean acid metabolism [CAM]) that influence the timing of stomatal opening and leaf water content may also affect MRT LW values and thus the sensitivity of a plant species to δ 18 O V variations (Cernusak et al, 2008;Dubbert, Kübert, & Werner, 2017;Liang et al, 2018). However, studies focusing on the influence of leaf functional traits on the equilibration between δ 18 O V and δ 18 O LW and thus MRT LW are scarce (Kim & Lee, 2011;Lai et al, 2008;Roden & Ehleringer, 1999 (Lehmann et al, 2018;Studer, Siegwolf, Leuenberger, & Abiven, 2015).…”