Tight stomatal regulation and high intrinsic capacity of carbon assimilation inferred from isotopic composition negatively correlate with drought-driven decline in sclerophyllous species

BACKGROUND AND AIMS: Long-term droughts reduce the carbon (C) and water pools of trees, causing mortality. However, the underlying physiological mechanisms explaining tree mortality remain unclear, and evidence from mature forests is scarce. The Chilean sclerophyllous forest has shown an abrupt and severe decline after >10 years of continuous drought, evidenced by browning and defoliation. We hypothesized that limited photosynthesis led to reduced concentrations of non-structural carbohydrates (NSC) and consequently impaired dehydration tolerance, and that drought resistance imposed a penalty in growth rates. METHODS: We quantified the species-specific level of crown decline in eleven woody species and sampled unhealthy and healthy individuals within species to measure isotopic composition (δ18O and δ13C) and NSC concentrations in twigs and leaves formed in 2019 and 2020 as well as mean basal area increment (BAI) before (1999-2009) and during the megadrought (2010-2020). The effects of species-specific crown decline and intraspecific health status on isotopes, NSC, and BAI were evaluated using linear mixed-effects models. KEY RESULTS: δ13C decreased with species' crown decline, while δ18O did not change, indicating biochemical limitations to C assimilation in species with higher decline. Stomatal limitations to C assimilation, inferred from higher δ18O, along with lower NSC and sugar concentrations, were found in healthy individuals of species with less crown decline and in unhealthy individuals of species with higher crown decline. Unhealthy individuals grew less than healthy ones in both periods examined and regardless of species' crown decline. CONCLUSIONS: Species' crown decline in the sclerophyllous forest of Central Chile was associated with biochemical and diffusive limitations on photosynthesis, but it was not related to reduced levels of NSC or to historical high or low growth rates. Results suggest that a timely stomatal regulation successfully prevents dehydration and reduces crown decline only when it occurs along with a high capacity of C assimilation.