Linking aboveground and belowground interactions via herbivore-induced plant volatiles

Plants mediate above-and belowground interactions within insect assemblages via herbivore-induced plant volatiles and thereby influence host plant colonization by different herbivores. By changing shoot-emitted volatiles, herbivores may disrupt the host location behavior of heterospecific herbivores and natural enemies. However, effects of simultaneous conspecific above-and belowground herbivory on multiple trophic levels have received little attention. First, we infested Chinese tallow tree plants with aboveground feeding adults and/or belowground feeding larvae of a beetle (Bikasha collaris) alone or together with heterospecific above-or belowground herbivores. Then, we determined the preferences of heterospecific above-and belowground herbivores plus an entomopathogenic soil nematode for these plants in greenhouse experiments and olfactometer trials. Finally, we used gas chromatography-mass spectrometry to analyze above-and below ground volatiles variation among different feeding treatments. We found that Spodoptera litura moths avoided plants with herbivory by B. collaris larvae and adults via herbivore-induced plant volatiles. The herbivorous belowground feeding grub Holotrichia parallela avoided plants with above-or belowground herbivory. The parasitic nematode Heterorhabditis megidis preferred plants that had B. collaris larvae. Furthermore, the profiles of both leaf and root volatiles induced by B. collaris larvae and adults plus other herbivores varied. These results hint that interactions involving above-and belowground conspecific herbivores could shape plant rhizosphere and phyllosphere herbivore communities by modifying above-and belowground volatiles, as well as by modulating colonization by other herbivores and associated natural enemies.