Does "enemy-free space" exist? Experimental host shifts of an herbivorous fly

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 suppo rt 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 cr eating a host shift for a specialized leaf mining By, Liriomyza helianthi ( Diptera: Agromyzidae). We manually transferred leafminer larvae from their normal host plant, Helianthus annuus (Asteraceae), to a variety of novel pl ants: Helianthus maximilianii, Ambrosia artemisiifolia, Taraxacum officinal e, 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 s pace. 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 tha n in the normal host. Nevertheless, there was significant within- and betwe en-year heterogeneity in results over the 3-yr period of the study. We foun d that escape from natural enemies was related to annual variation in the d iversity and abundance of parasitoid species. In years when parasitoid asse mblages 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 dev eloping in novel plants, a result that could be explained by the less discr iminating nature of the ectoparasitoids. When overall levels of mortality f rom natural enemies were high, the benefit of novel plants was also reduced . This pattern suggests that, as available larval hosts become scarce, para sitoids may be more likely to forage on novel host plants in search for pre y, thus diminishing the opportunity for enemy-free space. Nevertheless, our study showed that enemy-free space can exist for an herbi vorous insect utilizing a novel host plant, and that natural enemies may, i n some cases, offset physiological fitness costs often associated with deve loping in novel plants. If all else is equal, the balance of these factors may facilitate the inclusion of novel host plants into the feeding repertoi re of an herbivore.