Spittlebugs vs predators: the importance of incidental vibrations for the detection of threats by insect vectors of Xylella fastidiosa

The vibrational disruption of insect pests’ interaction with the environment is a new promising frontier in the control of either direct pest or insect vectors of plant pathogens. Reducing the frequency of insect–plant interactions leveraging on vibrational stimuli evoking the risk of predation could potentially affect the transmission rate of vector-borne plant pathogens as Xylella fastidiosa, whose main vector in Europe is the meadow spittlebug Philaenus spumarius. Here, we sought to address a fundamental question in the development of a behavioral manipulation strategy to disrupt spittlebug-mediated transmission of X. fastidiosa: are incidental vibrations emitted by predators a significant factor in spittlebugs’ risk detection? To respond to this question, we compared Philaenus spumarius response to hunting spiders collected in Apulian (southeastern Italy) olive orchards with the response to the sole spider vibrations recorded with a laser vibrometer and played back through a mini-shaker. A white noise and a leafhopper-emitted vibration were used as controls to evaluate spittlebugs’ response to vibrational signals not associated with a predation risk. In all trials, P. spumarius main response to spiders searching for the prey was freezing, i.e., cessation of any kind of activity. In playback trials, incidental vibrations alone emitted by spiders’ foraging triggered a freezing response in 63% of the tested spittlebugs; the duration of the freezing was approximately half of the duration of the behavior in response to the spider. Freezing was significantly more frequent in response to spider-foraging vibration (63%) than to the white noise and the leafhopper-emitted vibration (both 10%); no freezing was observed in the silent control. Overall, our findings suggest that substrate-borne vibrations are an important component of predation-risk assessment in P. spumarius. However, the perception and the response to a threat are likely multimodal processes mediated by the integration of vibrations with chemical and visual cues. Our results pave the way for the development of a behavioral disruption strategy against spittlebugs and X. fastidiosa transmission based on natural enemies-derived substrate-borne vibrations