Girdling behavior of the longhorn beetle modulates the host plant to enhance larval performance

Abstract

Abstract Background Preingestive behavioral modulations of herbivorous insects are abundant over insect taxa. Those behaviors are suspected to have functions such as deactivation of host plant defense, nutrient accumulation, or modulating plant-mediated herbivore interaction. However, the hypotheses have rarely been experimentally tested, especially at molecular level. To understand the functional consequence of behavioral modulation of insect herbivore, we studied the girdling behavior of Phytoecia rufiventris Gautier (Lamiinae; Cerambycidae) on its host plant Erigeron annuus L. (Asteraceae) that is performed before endophytic oviposition in the stem. Results The girdling behavior significantly increased the larval performance in both field monitoring and lab experiment. The upper part of the girdled stem exhibited lack of jasmonic acid induction upon larval attack, lowered protease inhibitor activity, and accumulated sugars and amino acids in compared to non-girdled stem. The modulated plant physiology allowed P. rufiventris larvae to allocate resources from detoxification to growth at the transcriptional level. The girdling behavior had no effect on the larval performance of a non-girdling longhorn beetle Agapanthia amurensis, which also feeds on the stem of E. annuus during larval phase. However, the girdling behavior decreased the preference of A. amurensis females for oviposition, which enabled P. rufiventris larvae to avoid competition with A. amurensis larvae. Conclusions In conclusion, the girdling behavior modulates plant physiology and morphology to provide a modulated food source for larva and hide it from the competitor. Our study implies that the insect behavior modulations can have multiple functions, providing insights into adaptation of insect behavior in context of plant-herbivore interaction.