Fall webworm host plant preferences create enemy-free space in its interaction with parasitoids

Abstract

Based on the “enemy-free space” hypothesis, in order to avoid natural enemies, insects may prefer host plants that are nutritionally suboptimal but are less visited by their natural enemies. The fall webworm, Hyphantria cunea Drury has more than 600 reported hosts. Chouioia cunea, a parasitoid wasp, is the main natural enemy of H. cunea. We addressed the question whether the preference of H. cunea for host plants correlate with attractiveness of the plants to C. cunea. H. cunea larvae were reared on leaves of eight different host plants, and the relationship between H. cunea host preference and preferences of the parasitic wasp were evaluated. The preferred host plant of female H. cunea was mulberry, Morus alba. Compared with other plants, M. alba was a poor nutritional host for H. cunea. However, compared with other host plants, M. alba attracted fewer natural enemies C. cunea. GC-MS combined with GC-EAD analysis revealed six compounds in the volatiles of different plant HIPVS after feeding by H. cunea. Behavioral assays showed that tridecane alone did not elicit any attraction or repellency responses of the host H. cunea or the parasitoid C. cunea. When tridecane was mixed with other HIPVS, however, the mixture could attracted C. cunea and repelled H. cunea. Notably, only M. alba HIPVS did not contain tridecane. Thus, H. cunea exploits M. alba as an enemy-free space, minimizing attacks by the parasitoid C. cunea. This information underscores that adaptive responses of herbivores need to be considered in the context of multi-trophic relationships rather than optimizing herbivore growth on the most nutritionally adaptive plant host.