Functional investigation of monoterpenes for improved understanding of the relationship between hosts and bark beetle

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.