A rationale for chemical defense mixtures in spruce oleoresin: most monoterpenes are highly toxic to either bark beetles or to their symbiotic fungi, but not both

Abstract

1. Chemical defenses, such as the monoterpenes of conifer oleoresin frequently occur as complex blends of many components, but the underlying ecological reasons for these mixtures are not yet known. Several theories attempt to explain the existence of chemical defense mixtures in plants. However, due to limited empirical evidence, it is unclear which theories might best apply. 2. Here, we tested the bioactivity of 12 individual Norway spruce monoterpenes and their mixtures to adult Eurasian spruce bark beetles, Ips typographus, and three major symbiotic fungi in the vapor phase using survival and growth bioassays. Next, we evaluated whether spruce trees could alter their monoterpene profile in response to fungal infection. 3. Individual monoterpenes had generally opposite effects on bark beetles compared to symbiotic fungi. The compounds that were most toxic to beetles were the least inhibitory to fungal growth and vice versa. The least abundant monoterpenes had the strongest bioactivity against both beetles and fungi, while the most abundant monoterpenes showed intermediate bioactivity. Among the symbiotic fungi tested, one (Grosmannia penicillata) exhibited high tolerance to monoterpenes, and its growth was even stimulated by the monoterpenes most toxic to the beetle. Interestingly, spruce bark responded to G. penicillata inoculation by accumulating higher concentrations of specifically fungistatic monoterpenes. 4. Our results support the interaction diversity hypothesis, which posits that defense mixtures are maintained in plants because the individual components target different attackers. The monoterpene identity and concentration together determine the effectiveness of these compounds against herbivores and pathogens.