Aphids Facing Their Parasitoids: A First Look at How Chemical Signals May Make Higher Densities of the Pea Aphid Acyrthosiphon pisum Less Attractive to the Parasitoid Aphidius ervi

SIMPLE SUMMARY: Successful foraging behavior of parasitoids depends on specific organic information emitted by host-infested plants. For instance, the emission of volatile compounds increases in infested plants, and these are the first indicator of host presence. Parasitoids are attracted by these volatiles in a quite specific way. By combining behavioral and chemical studies, we showed bottom-up effects in a broad bean Vicia faba (Fabaceae)–pea aphid Acyrthosiphon pisum (Homoptera: Aphididae)–parasitoid Aphidius ervi (Hymenoptera: Braconidae) model system. We found that behavioral selection of parasitoid females toward plants with a high density of aphid infestation was reduced, and this can be linked to reduced emission of volatile compounds. In practice, if parasitoids are less attracted to plants with high-density aphid infestations, there may be potential negative impacts on biological control. Therefore, the common recommendation in biological control is to release parasitoids early in the season when aphid density on crop plants is still low. ABSTRACT: Herbivore-induced plant volatiles constitute the first indicators of insect host presence, and these can affect the foraging behavior of their natural enemies. The density of insect hosts may affect the nature and concentration of these plant-induced volatiles. We tested the impact of infestation density (low, intermediate, and high) of the pea aphid, Acyrthosiphon pisum (Homoptera: Aphididae), feeding on the broad bean Vicia faba, on the attractiveness of the parasitoid Aphidius ervi (Hymenoptera: Braconidae), using a Y-tube olfactometer (infested vs. non-infested plants). The emitted volatile compounds from both infested and non-infested plants were collected and identified. In addition, two series of experiments were carried out to test the impact of the presence of a conspecific female parasitoid within the aphid/plant complex on the attractiveness to other females. Parasitoids were significantly more attracted to the plants with low and intermediate aphid infestation levels. The volatile blend composition of the infested plants changed in relation to aphid density and may explain the low attraction of parasitoids toward high aphid density. The presence of conspecific females on the aphid patch had no apparent impact on the behavioral choices of other parasitoid females. Our study adds a new aspect to understanding plant–aphid–parasitoid interactions, including the possibility that aphids may manipulate chemical cues of host plants affecting the orientation of parasitoids.