Dendroanatomy of xylem hydraulics in two pine species: Efficiency prevails on safety for basal area growth in drought-prone conditions

Xylem structure optimizes water conductivity while preventing hydraulic failure via embolism resistance, but how this process is modulated by climate variability and how it affects secondary growth in mature trees is still not fully understood, particularly in water-limited environments. Using quantitative wood anatomy techniques, we estimated xylem anatomical proxies for hydraulic efficiency (xylem specific conductivity, Ks) and safety (cell wall reinforcement, wrein) in two western US conifers, Pinus flexilis and Pinus longaeva, at a montane and subalpine location respectively. We built two large datasets (570 rings for P. flexilis, 635 rings for P. longaeva) to investigate 1) the variability of anatomical parameters (i.e lumen diameter, cell wall thickness) and hydraulic proxies along the stem in the five outermost rings (2009–2013); 2) the response of hydraulic proxies to daily climate over a period of 24 years (1990–2013); and 3) the relationship between xylem hydraulic architecture and basal area increment (BAI). Lumen diameter scaled along the stem following a power function, but the scaling patterns of cell wall thickness and hydraulic proxies differed significantly between species. From 1990–2013, Ks decreased in both species, whereas wrein increased only in P. longaeva, while no trends were observed in BAI. Climate sensitivity of Ks peaked over a longer period (84–102 days) compared to wrein (20–55 days), responding to increasing minimum temperature. In both species, Ks was a better predictor of BAI than wrein, indicating that, even under severely water-limited conditions, radial growth is linked to hydraulic efficiency rather than safety. Based on the variability of cell density along the stem, the trade-off between hydraulic efficiency and safety in P. longaeva appeared to be controlled by a strategy of space occupation. Characterizing the mechanistic relationship between xylem anatomy, plant hydraulic functioning, and stem growth is necessary to better understand climate-growth relationships in the western US and species' growth plasticity under future climate change scenarios.