Synergies between hydraulic safety and efficiency reduce tree susceptibility to insect attack

The tight coupling between drought and insect attack threatens trees in a warmer world. Trees with differing levels of hydraulic safety and efficiency likely have different susceptibilities to insect attack, but how hydraulic architecture of woody tissues moderates the relationship between drought and insects remains unknown at the species scale. Here, we test how hydraulic safety and efficiency, derived from anatomical and isotopic measurements of the stem xylem, coordinate to regulate growth and survival of whitebark pines in the Rocky Mountains, USA. We assess intraspecific and ontogenetic variability in xylem hydraulic traits by comparing between trees that survived or were killed during a mountain pine beetle outbreak. At the individual tree scale, we found synergies between safety and efficiency: at the time of the outbreak, trees with higher cell-wall reinforcement and wood density (safety) also had higher average theoretical hydraulic conductivity and carbon-use efficiency (efficiency), and this was associated with higher growth, carbon storage, and survival. At the annual timescale, however, we found tradeoffs between safety and efficiency: higher safety was associated with lower efficiency for 7 of 9 pairwise comparisons. Yet, years that maximized both safety and efficiency showed the most tree growth and carbon storage. The xylem hydraulic traits underlying tree growth and survival were not stationary over time, but prominent differences at the time of the outbreak suggest that both higher hydraulic safety and efficiency were positively associated with resistance against bark beetles. The importance of hydraulic traits to tree survival suggest that tree responses to increasing herbivory will depend on tree responses to climate warming and hydrological changes as well.