Spruce bark beetle (Ips typographus L.) is the most destructive insect pest of spruce forest in Eurasia. However, contact toxicity, in vivo metabolism, and ecological functions of host monoterpenes are poorly understood at the spruce–bark beetle–predator tritrophic level. Spruce monoterpenes including S-(–)-α-pinene, R-(+)-α-pinene, and myrcene showed contact toxicity to spruce bark beetle, with LD50 values ranging from 24–36 μg/mg. When topically treated with S-(–)-α-pinene or R-(+)-α-pinene, the amount of volatile metabolites [S-(–)-cis-verbenol, 4S-(+)-/4R-(–)-trans-verbenol, and R-(+)-/S-(–)-verbenone] in the hindgut extract of spruce bark beetle varied significantly between sexes, and their quality varied significantly depending on the chirality of α-pinene. More importantly, S-(–)-α-pinene induced male adults to produce large amounts of S-(–)-cis-verbenol and S-(–)-verbenone. When topically treated with myrcene, the expected semiochemicals such as E-myrcenol, ipsenol, and ipsdienol were not detected in beetle hindgut, indicating that the pheromone biosynthetic system of spruce bark beetle does not participate in the metabolism of host myrcene. In the field trapping tests, S-(–)-α-pinene and R-(+)-α-pinene increased the trap catches of spruce bark beetle and Thanasimus substriatus (predator) compared with the pheromone source, whereas myrcene exhibited a strong repellent effect on bark beetle but not on its predator. Our results of contact toxicity, in vivo metabolism, and behavioural activity analyses indicate that spruce bark beetle adopts different ecological strategies to adapt to and tolerate different host monoterpenes; for example, avoidance mechanism for myrcene, and preference mechanism for α-pinene. Signalling interactions among the three monoterpenes at the tritrophic level help us understand their roles in manipulating the arms race between host plants and bark beetles, which indicate the plasticity and multifunctionality of host monoterpenes in the ecological context. Our results can be applied to the management of spruce bark beetle via the push-pull strategy using semiochemicals.

Data set collected by count mortality of Ips typographus after monoterpenes topically treated, and the volatiles in hindguts were identification and analysis by GC and GC-MS.