Die-off after an extreme hot drought affects trees with physiological performance constrained by a more stressful abiotic niche

• Multifunctional analysis of tree die-off combining observations and modeling. • There was abiotic niche differentiation between dead and surviving trees. • The soil niche likely determined the tree functional strategy prior to mortality. • Trees are increasingly sourcing for deeper water to buffer climate change. • Dead trees expressed a functional scale paradox in response to water stress. Forest die-off has become more frequent under climate change, making crucial to understand the physiological mechanisms of forest mortality. We analyzed Quercus ilex die-off after a record-setting hot drought in two open woodlands without previous signs of decline. To understand physiological performance of trees we compared observations of radial growth dynamics, xylem hydraulic architecture, sapwood nutrient content and δ 13 C and δ 18 O in wood cellulose, with model simulations of tree carbon and water fluxes. We also assessed climate-growth responses across a Q. ilex network including sites with and without increased mortality. Past extreme droughts triggered multidecadal growth declines consistently in dead trees, which suggests long-term vulnerability of dead Q. ilex independent of the mortality process or causal factor. In the two studied woodlands, trends in xylem cellulose δ 18 O suggest that both dead and surviving trees increasingly relied on deeper water sources as stress increased under climate change. Dead and surviving trees followed different functional strategies reflecting chronic abiotic niche-related differences in stress. Dead trees invested similar or larger amounts of carbon in xylem reservoir tissues and less in xylem conductive tissues compared to surviving trees, yet exhibited an impaired nutrient status. Xylem hydraulic architecture differed in surviving and dead trees. The latter formed more efficient xylems with higher vessel density and larger or similar vessel sizes. The isotopic proxies suggested that dead trees systematically maintained tighter stomatal regulation and were forced to rely on deeper water likely sourced from the fractured granite bedrock. Isotopic proxies and simulations of water and carbon dynamics further suggest that surviving trees benefitted from soils with higher water-holding capacity contributing to buffer water stress. Dead trees expressed a functional paradox. Although their long-term functional strategy successfully coped with higher baseline water stress, they failed to withstand the additional increase in stress during an unprecedented hot drought.