Gall-forming aphids are protected (and benefit) from defoliating caterpillars: the role of plant-mediated mechanisms

Background: Interspecific interactions among insect herbivores are common and important. Because they are surrounded by plant tissue (endophagy), the interactions between gall-formers and other herbivores are primarily plant-mediated. Gall-forming insects manipulate their host to gain a better nutrient supply, as well as physical and chemical protection form natural enemies and abiotic factors. Although often recognized, the protective role of the galls has rarely been tested. Results: Using an experimental approach, we found that the aphid, Smynthurodes betae, that forms galls on Pistacia atlantica leaves, is fully protected from destruction by the folivorous processionary moth, Thaumetopoea solitaria. The moth can skeletonize entire leaves on the tree except for a narrow margin around the galls that remains intact (“trimmed galls”). The fitness of the aphids in trimmed galls is unharmed. Feeding trials revealed that the galls are unpalatable to the moth and reduce its growth. Surprisingly, S. betae benefits from the moth. The compensatory secondary leaf flush following moth defoliation provides new, young leaves suitable for further gall induction that increase overall gall density and reproduction of the aphid. Conclusions: We provide experimental support for the gall defense hypothesis. The aphids in the galls are protracted by plant-mediated mechanisms that shape the interactions between insect herbivores which feed simultaneously on the same host. The moth increase gall demsity on re-growing defoliated shoots.