DOES “ENEMY-FREE SPACE” EXIST? EXPERIMENTAL HOST SHIFTS OF AN HERBIVOROUS FLY

Abstract

Natural enemies have been proposed as important agents of natural selection on herbivorous insects that may facilitate host plant shifts and increases in diet breadth. However, there is little experimental field work to support claims of host-shifting via escape from natural enemies, i.e., to enemy-free space. In this study, we took the unique approach of experimentally creating a host shift for a specialized leafmining fly, Liriomyza helianthi (Diptera: Agromyzidae). We manually transferred leafminer larvae from their normal host plant, Helianthus annuus (Asteraceae), to a variety of novel plants: Helianthus maximilianii, Ambrosia artemisiifolia, Taraxacum officinale, and Centaurea solstitialis. By exposing transferred larvae on normal and novel plants to natural enemy attack under field conditions, we were able to examine whether host-shifting can provide an herbivore with enemy-free space. Our data show that enemy-free space does exist for L. helianthi immediately following a host shift, as mortality in novel plants averaged 17% less than in the normal host. Nevertheless, there was significant within- and between-year heterogeneity in results over the 3-yr period of the study. We found that escape from natural enemies was related to annual variation in the diversity and abundance of parasitoid species. In years when parasitoid assemblages were dominated by endoparasitoids, mortality of larvae averaged 22% lower in novel hosts. However, when generalist ectoparasitoids, Diglyphus spp. (Hymenoptera: Eulophidae), were present, there was no advantage of developing in novel plants, a result that could be explained by the less discriminating nature of the ectoparasitoids. When overall levels of mortality from natural enemies were high, the benefit of novel plants was also reduced. This pattern suggests that, as available larval hosts become scarce, parasitoids may be more likely to forage on novel host plants in search for prey, thus diminishing the opportunity for enemy-free space. Nevertheless, our study showed that enemy-free space can exist for an herbivorous insect utilizing a novel host plant, and that natural enemies may, in some cases, offset physiological fitness costs often associated with developing in novel plants. If all else is equal, the balance of these factors may facilitate the inclusion of novel host plants into the feeding repertoire of an herbivore.