Two-step learning involved in acquiring olfactory preferences for plant volatiles by parasitic wasps

Aphidius ervi is a parasitic wasp of several aphid species, including Acyrthosiphon pisum. This wasp is used as a biological control agent of its host aphid species in many regions of the world. Compared with responses to volatiles from intact plants, A. ervi females respond to host-infested plant volatiles but not to nonhost-infested plant volatiles. Furthermore, we previously demonstrated that A. ervi preferred host aphid-infested plant volatiles to volatiles from intact plants only when they had been exposed to the host aphid-infested plant volatiles during their developmental stages (larval to emergence stages). The results suggested that A. ervi females learn the host-infested volatiles during their development and we tested this hypothesis in this study. Learning occurred in two steps: during the late larval to prepupal stages (the first learning stage) and during adult emergence (the second learning stage). Furthermore, we observed specificity to the host plant volatiles in the two-step learning. The preference for host-infested plant volatiles was modified when the wasps had been exposed to host aphid-infested plant volatiles in the first stage and then exposed to nonhost aphid-infested plant volatiles in the second stage. When they were exposed to nonhost aphid-infested plant volatiles in the first stage, wasp preference for volatiles was not detected, irrespective of their exposure to either host or nonhost aphid-infested plants in the second stage. The ecological functions of the two-step learning are discussed.