We evaluated the ability of constitutive and inducible defenses to protect trees and restrict herbivore reproduction across the endemic, incipient (i.e., transitory), and eruptive phases of a native bark beetle species. Host defenses were major constraints when mountain pine beetle (Dendroctonus ponderosae Hopkins) populations were low, but inconsequential after stand-level densities surpassed a critical threshold. We annually examined all lodgepole pines (Pinus contorta Douglas var. latifolia) in six 12–18 ha stands for 3–6 years for beetle attack and establishment as beetle densities progressed through various population phases. We also assayed a suite of tree physiological and chemical attributes and related them to subsequent attacks during that year. Rapidly inducible defenses appeared more important than constitutive defenses, and total monoterpenes were more important than particular constituents. Trees that exude more resin and accumulate higher monoterpene concentrations in response to simulated attack largely escaped natural attacks when populations were low. In stands where beetles had reached incipient densities, these defenses were ineffective. Larger diameter trees had more pronounced defenses than smaller diameter trees. As populations increased, beetles selected increasingly larger, more resource-rich trees, despite their better defenses. When populations were too low for cooperative attack, beetles exploited trees weakened by lower-stem insects. Behavioral plasticity allows beetles to persist at endemic levels until conditions shift, after which positive feedbacks predominate.

Bark beetles encounter a diverse array of constitutive and rapidly induced terpenes when attempting to colonize living conifers. Concentrations of these compounds at entry sites can rapidly reach levels toxic to beetles, their brood, and fungal symbionts. Large numbers of beetles can overwhelm tree defenses via pheromone-mediated mass attacks, but the mechanisms are poorly understood. We show that bacteria associated with mountain pine beetles can metabolize monoterpenes and diterpene acids. The abilities of different symbionts to reduce concentrations of different terpenes appear complementary. Serratia reduced concentrations of all monoterpenes applied to media by 55-75 %, except for α-pinene. Beetle-associated Rahnella reduced (-)- and (+)-α-pinene by 40 % and 45 %, respectively. Serratia and Brevundimonas reduced diterpene abietic acid levels by 100 % at low concentrations. However, high concentrations exhausted this ability, suggesting that opposing rates of bacterial metabolism and plant induction of terpenes are critical. The two major fungal symbionts of mountain pine beetle, Grosmannia clavigera and Ophiostoma montium were highly susceptible to abietic acid. Grosmannia clavigera did not reduce total monoterpene concentrations in lodgepole pine turpentine. We propose the ability of bark beetles to exert landscape-scale impacts may arise partly from micro-scale processes driven by bacterial symbionts.