Plants respond to leaf vibrations caused by insect herbivore chewing

Abstract

Plant germination and growth can be influenced by sound, but the ecological significance of these responses is unclear. We asked whether acoustic energy generated by the feeding of insect herbivores was detected by plants. We report that the vibrations caused by insect feeding can elicit chemical defenses. Arabidopsis thaliana (L.) rosettes pre-treated with the vibrations caused by caterpillar feeding had higher levels of glucosinolate and anthocyanin defenses when subsequently fed upon by Pieris rapae (L.) caterpillars than did untreated plants. The plants also discriminated between the vibrations caused by chewing and those caused by wind or insect song. Plants thus respond to herbivore-generated vibrations in a selective and ecologically meaningful way. A vibration signaling pathway would complement the known signaling pathways that rely on volatile, electrical, or phloem-borne signals. We suggest that vibration may represent a new long distance signaling mechanism in plant-insect interactions that contributes to systemic induction of chemical defenses.

Fig. 1

a Vibrations produced by a feeding P. rapae caterpillar on A. thaliana, recorded simultaneously (using two laser vibrometers) on the fed-upon leaf and a second leaf on the opposite side of the plant. These leaves correspond to the leaves labeled ‘pbl’ and ‘sl’ in the playback design shown in the next panel. b Sampling design for the experiments. An older leaf was selected for caterpillar recordings and vibrational playback (pbl), to allow attachment of an actuator with minimal effect on the rest of the plant. For the plants that experienced herbivory (all of the plants in experiment 1, and half of the plants in experiment 2), caterpillars were confined in clip cages placed on the playback leaf and a same-age leaf on the opposite side of the plant (sl). The two leaves experiencing herbivory 24 or 48 h after the experimental treatment are marked with an asterisk. The young unexpanded leaves in the rosette center (rc) were also sampled for leaf chemistry, but did not experience herbivory

Fig. 2

a Playback of caterpillar feeding vibrations increased the induced response of A. thaliana to herbivore damage, compared to no-vibration controls (*p < 0.05, error bars 95 % confidence intervals; there was no difference between the 24 and 48 h samples, so they were pooled here). N = 44 per bar (43 for rosette center). b Grayscale map showing the increase in aliphatic glucosinolates in the playback and same-age systemic leaves, expressed as the percent change from the levels in controls

Fig. 3

Relationship between the amplitude of the chewing vibration exemplars used in playbacks and the level of induced aliphatic GS. Linear regression, N = 22

Fig. 4

a Chewing vibrations increased the anthocyanin response to herbivory by A. thaliana ( the ratio of response in fed-upon plant vs. non-fed-upon plant, when both had same treatment exemplar). Error bars 95 % CI. Letters above bars indicate that the response to the chewing treatment was significantly different (p < 0.001) from responses to the three controls. b Averaged amplitude spectra of the stimuli used in the experiment (N = 18 for each stimulus type) suggest that chewing can be distinguished from wind, but not from leafhopper song, based on the frequency content. c Vibration waveforms of a chewing P. rapae caterpillar on A. thaliana; wind on A. thaliana; and a leafhopper, recorded on another host plant. Chewing and leafhopper song have similar amplitude spectra but different temporal features