Eavesdropping plants: Plants perceive and respond to insect odors by priming their anti-herbivore defenses

Insect feeding damage is known to induce plant defenses. More recent discoveries have found that plants can also perceive environmental cues associated with the presence of insect herbivores, allowing them to prepare their defenses for future attack. For example, plants can detect insect footsteps or oviposition, and some even use olfactory cues to sense the presence of nearby herbivores. Several studies have found that undamaged plants eavesdrop on volatiles emitted by their insect-damaged neighbors and respond by enhancing their own anti-herbivore defenses. In my dissertation research, I demonstrate for the first time that plants can also perceive and respond to olfactory cues emitted directly by insect herbivores. My findings indicate that tall goldenrod (Solidago altissima) plants exhibit enhanced defense responses following exposure to the putative sex attractant of a specialist herbivore, the goldenrod gall fly (Eurosta solidaginis).;In field and laboratory experiments, goldenrod plants previously exposed to the male fly emission suffered significantly less herbivore damage than unexposed controls. Moreover, goldenrod plants exposed to the fly odor induced higher amounts of the key defense signaling hormone jasmonic acid and emitted greater quantities of defenserelated volatile compounds following herbivore damage. I also found that exposure to the E. solidaginis emission does not directly deter subsequent insect feeding as exposing other plant species to the emission did not reduce herbivore feeding damage.;Because little is known about how plants perceive olfactory cues and the specificity of plant olfaction, I also investigated S. altissima responses to the individual chemical constituents of the E. solidaginis emission blend. I found that goldenrod plants exposed to the most abundant compound in the blend, (7S,5 S)-7-methyl-1,6- dioxaspiro[4.5]decane, received less herbivore damage and induced higher quantities of jasmonic acid than control plants, a similar result to plants exposed to the complete blend.;Male E. solidaginis flies emit very large quantities of the putative sex attractant (~70 +/- 20 mug over 24 h), despite providing a cue for eavesdropping S. altissima plants. To determine whether female E. solidaginis may select for this trait and whether emission production is correlated with E. solidaginis male quality, I quantified the amount of emission produced as well as other physical characteristics of individual male flies, such as mass, gall-size, and life span. I found that emission production is not correlated with gall size, male mass, or life span. However, I did observe that the ratio of compounds in the male emission changes with fly age.;Together, these results suggest that S. altissima plants eavesdrop on the olfactory signals of their insect antagonist and exploit these signals as indicators of impending herbivory. These findings document a new class of olfactory-mediated interactions with broad significance for the evolutionary ecology of plant-insect interactions.