Oviposition Preference and Performance of a Specialist Herbivore Is Modulated by Natural Enemies, Larval Odors, and Immune Status.

Insect herbivores frequently must balance host plant quality and the risk of attack by their natural enemies when making oviposition decisions. Yet, which factor is more important remains unresolved in plant-insect ecology. Here, we report the oviposition preference and larval performance of the brassicaceous specialist Plutella xylostella, in the context of plant quality (cabbage Brassica oleracea vs. mustard B. juncea) and associated natural enemies. Despite the greater larval weight and adult lifespan on cabbage, ovipositing females strongly preferred mustard. Both the egg parasitoid Trichogrammatoidea bactrae and the larval ectoparasitoid Bracon brevicornis are more likely to attack P. xylostella that feed on cabbage; thus, mustard represents enemy-reduced space from these two parasitoids. However, larval diet had no impact on the parasitism rate of specialist Cotesia vestalis. Feeding on mustard improved larval immune responses. The total hemocyte number, diversity, and phenoloxidase activity were higher in mustard-fed larvae which increased their survival against the entomopathogen, Bacillus thuringiensis. Interestingly, host plants altered the larval body odor profile. Mustard-fed larvae emitted allyl isothiocyanate (AITC) and butyl isothiocyanate (BITC) while cabbage-fed larvae emitted dimethyl disulphide (DMDS) and dimethyl trisulphide (DMTS) that served as short-range cues for larval parasitoids. For B. brevicornis, host body odor guided oviposition choice was crucial as their fitness was affected by the host larval diet. Although C. vestalis showed a clear preference towards volatiles emitted by mustard fed larvae, their fitness was unaltered. Taken together, our results illustrate that P. xylostella prefers to lay eggs on mustard plants providing enemy-reduced space from some, but not all, natural enemies.