For a Limited Time Only? How Long Can Trees Maintain Enhanced Chemical Defenses During Pre-Mortality Heat and Drought Stress

The relative contribution of forest pests to climate and drought-induced tree mortality is complex and largely absent from current process-based models. Recent efforts have focused on developing frameworks to integrate insects into models of tree mortality, citing the need for a better mechanistic understanding of the links between stress-induced tree physiology and insect behavior and population dynamics. Secondary plant metabolites (SPMs) play a critical role in plant resistance and their synthesis and mobilization are coupled to carbon assimilation, hydraulic conductivity, and herbivory itself. Insect host choice also depends in part on behavioral responses to host SPMs. Monoterpenes are the dominant SPMs in conifers, and while high concentrations of monoterpenes are toxic to bark beetles, lower concentrations serve as precursors for a number of aggregation pheromones. Thus, the impact of monoterpenes on bark beetle behavior is complex and is impacted by environmental effects on primary metabolism including heat and drought stress. Here, we quantify the dynamics of piñon pine monoterpene chemistry as a function of predicted and prolonged drought stress implemented at the SUrvival MOrtality (SUMO) experimental site at the Los Alamos National Laboratory, NM, USA. In both woody and needle tissues, total monoterpene concentrations in ambient trees were not significantly different from those observed in trees exposed to heat stress, but drought trees showed higher total concentration while heat+drought trees were observed to have the highest levels (2 fold increase over ambient). These treatment effects were sustained over a two-year period despite seasonal variation in tree water status; however, total concentration in the xylem and phloem were closely coupled to tree water potential and treatment effects took longer to manifest relative to the needles. Individual compounds responded differently to the treatments, suggesting cyclase-level enzyme regulation, while α-pinene - an important bark beetle aggregate pheromone precursor - dominated total monoterpene concentration dynamics. These results have important implications for piñon-bark beetle interactions during drought and provide a missing link between drought-induced physiology and insect behavior.