Aphid-induced plant volatiles affect the attractiveness of tomato plants to Bemisia tabaci and associated natural enemies

An in‐depth understanding of plant‐mediated interactions between herbivores and their natural enemies is essential in community ecology and co‐evolution, and for developing sustainable pest management strategies. The influence of Myzus persicae (Sulzer) (Hemiptera: Aphididae)‐induced tomato plant [Solanum lycopersicum L. (Solanaceae)] volatile compounds on the olfactory responses of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), three predator species [Coccinella septempunctata L., Propylea japonica (Mulstant) (both Coleoptera: Coccinellidae), and Orius sauteri (Poppius) (Hemiptera: Anthocoridae)], two whitefly parasitoid species [Encarsia formosa (Gahan) and Encarsia sophia (Girault & Dodd) (Hymenoptera: Aphelinidae)], and one aphid parasitoid species [Aphidius gifuensis Ashmead (Hymenoptera: Aphidiidae)] were examined in two‐choice tests using a four‐arm olfactometer. Tomato plants were experimentally manipulated for aphid density, duration of aphid feeding, and interval between aphid removal and the behavioral test. We also compared the systemic effects of aphid feeding on the olfactory behavior of whiteflies and natural enemies according to three relative leaf positions: the aphid‐infested leaf itself and two adjacent leaves (above and below). Bemisia tabaci were deterred by the odors of the leaves infested with aphids in all treatments. All six natural enemies were attracted to the leaves infested with aphids. Bemisia tabaci deterrence by volatiles was greater for leaves at the highest aphid density, and with increasing duration of exposure to aphid feeding. In contrast, the attraction to leaves was greater for the three parasitoids than for the three predators both with increasing aphid density and increasing duration of plant exposure to aphids. There was no significant influence of leaf position on preference of B. tabaci, the two species of lady beetles, and the aphid parasitoid. The two Encarsia species were attracted to the leaf above the aphid‐infested leaves, indicating that systemic volatiles were released by adjacent leaves. On the other hand, O. sauteri was only attracted by the aphid‐infested leaf itself. Our results showed that M. persicae‐infested host plants emitted volatiles that could inhibit the colonization by B. tabaci and also attract natural enemies of both aphids and whiteflies. The results of this study may need to be considered further for optimizing pest management methods.