Insect vibrational communication: description, decoding, and manipulation

Vibrations are extremely widespread and ancient among animals’ communication modalities; nevertheless, their importance has been neglected for many years. During my PhD I wanted to increase the knowledge about the role of vibrational signals in insects. Therefore, I conducted behavioral bioassays and laser vibrometer recordings to describe and decipher vibrations produced by four species belonging to two different orders. The role of vibrational signals in intraspecific communication varies widely among different groups of insects. For this reason I chose to study two model groups, Hemiptera and Hymenoptera. Hemiptera, in particular leafhoppers, rely almost exclusively on vibrations for intraspecific communication. Their reproductive strategy is based on the production of vibrational calling and courtship signals, which are necessary for identification and location of the mating partner. Similarly, male-male competition for mating is regulated by means of specific vibrational signals, which in many cases are used to interfere with an ongoing mating duet. The emission of specific disruptive noise gives the rival male a chance to access mating by replacing the calling male in the duet. Recent studies showed that disruptive signals can be played back into plants to effectively disrupt the mating behavior of the grapevine leafhopper, Scaphoideus titanus. These findings inspired my research, its aims and the experimental approach. First, I described and decoded the reproductive strategy and associated vibrational signals of two grapevine leafhoppers species, the green leafhopper, Empoasca vitis and the glassy-winged sharpshooter, Homalodisca vitripennis. Secondly, I used the acquired knowledge to select potential synthetic ‘disruptive signals’ and test their efficacy in disrupting the mating process of E. vitis in laboratory conditions. Hymenoptera, on the other hand, such as paper wasps of the genus Polistes, use mainly semiochemicals to coordinate colony activities (e. g., to discriminate among individuals and their roles). However, the “mechanical switch hypothesis” suggested that vibrations produced by body oscillation movements of foundresses can bias larvae development towards a worker phenotype. That is, when a larva is subjected to low frequency vibrations it will develop into a worker. The social parasite - host system, Polistes sulcifer – P. dominula, was a very good model to investigate the potential caste determination function of body oscillation movements in paper wasps. P. sulcifer, the parasite, does not have a worker caste and its reproductive success rely exclusively on the brood cares provided by the host workers that emerge from usurped colonies. For this reason, I described and compared the vibrations transmitted to the nest by both species in usurped and not-usurped colonies. Moreover, the “mechanical switch hypothesis” predicts that vibrations manipulate larval development by modulating the “nutritional effect” (i.e. larvae that are fed more should develop into reproductive individuals and viceversa). Therefore, I tested the P. dominula foundress ability to modulate the vibration emission in association or not with the feeding activity. This research unveiled remarkable information in both model groups. Several original aspects in the leafhopper mating behavior have been discovered. Main peculiarities have been found in the daily activity and the potential role of visual stimuli in E. vitis, and in the complex structure of signals and male-male rivalry interactions in H. vitripennis. These results showed that multimodal communication (i.e. vision plus vibrations) and ecological adaptations still need to be studied in leafhoppers to fully understand how vibrational signals evolved and adapted to ecological constraints. From an applied point of view, we identified one disruptive signal that, in laboratory conditions, was highly effective in disrupting E. vitis mating process. On the other hand, I described, for the first time in detail, the spectral properties of induced vibrations into a paper wasps nest produced by P. dominula and its social parasite P. sulcifer. By comparing the vibrations produced by P. dominula, in different larval nutritional conditions, and the parasite we found several significant differences. For example, the foundress varies the spectral and temporal properties when she is feeding the larvae; while the parasite produces vibrational events with some exaggerated features compared to the host (i.e. each event is composed of a higher number of pulses). Results have been discussed from an adaptive point of view considering the putative role of vibrations in leading larvae caste determination. Overall, this thesis provides novel insights on the great variability of functions and adaptations of vibrational signals. The acquired knowledge can be used as a basis to perform further experiments on biological and applied aspects of biotremology.