Narrower xylem vessels linked to tree decline risk during a recent drought-induced decline event

Abstract Drought-induced tree mortality and dieback is expected to become an increasingly significant issue as climate change increases the frequency, severity and duration of droughts. The primary proposed mechanism of drought-induced decline is hydraulic failure, which is mechanistically linked to xylem architecture. However, annual variation of xylem anatomical traits has largely been overlooked as a possible driver of tree decline, with a focus instead on traditional ring-width based dendrochronological methods. Here, we employ a quantitative wood anatomy approach to examine whether differences in xylem vessel lumen area were related to decline risk during a recent drought-induced decline of chestnut oak (Quercus prinus) from Southern Indiana, USA. Our results show that over at least the past 60 years, healthy trees built consistently wider vessels than those that succumbed. This phenomenon has now been observed across three continents, and in both tracheid- and vessel-bearing species, indicating that conduit size may be related to drought survival, likely as an indicator of long-term stress. Moreover, an analysis of the sensitivity of vessel lumen area to climate variables suggests that early winter warming may promote the production of wider vessels in the following year. In contrast, a negative correlation between prior year growing season length and vessel lumen area suggests that extended growing seasons may lead to narrower, potentially more vulnerable xylem vessels. These effects were less pronounced in the declining trees, hinting that already-stressed trees were less sensitive or physiologically unable to respond to climatic variability. Designing studies aimed at understanding the drivers of intra-specific variation in xylem conduit architecture could improve our ability to predict tree dieback and mortality under future climate scenarios.