Ecologists have labored to find an explanation for the lack of a positive correlation between host preference and offspring performance in herbivorous insects. This study focuses on how one herbivore species can influence another herbivore species ability to accurately assess the suitability of different host-plant genotypes for larval development. In particular, we examined the role that an early season xylem-feeding homopteran (meadow spittlebug, Philaenus spumarius) has on the preference-performance correlation of a late-season dipteran stem galler (Eurosta solidaginis) among different goldenrod genotypes. In a greenhouse, we released adult stem gallers into replicate cages that contained ramets from 4 different goldenrod genotypes crossed with 3 densities of spittlebugs (0, 1, or 8 nymphs placed 2 weeks previously on each ramet). Spittlebug feeding caused a density-dependent decline in ramet growth rates, which in turn caused a corresponding decrease in host-plant preference by the stem gallers (number of ovipunctures per bud or proportion of ramets attacked). Goldenrod genotype and the interaction between spittlebugs and genotypes also influenced host-plant preference by the stem galler.
Goldenrod genotype had the greatest impact on stem galler offspring performance (gall size or survivorship). Spittlebug density also affected performance, but only through its interaction with goldenrod genotype. On some genotypes, the survivorship of stem-galler larvae decreased with increasing spittlebug density, while on other genotypes, survivorship remained unchanged, or actually increased, with increasing spittlebug density. This suggests that there was genetic variance among goldenrod genotypes in their norms of reaction for their suitability as a host to the stem gallers. One possible explanation for why spittlebugs caused a significant reduction in preference, but not in performance, was that spittlebugs had very few long-term effects on the host plant. Flower number, flowering phenology, and the allocation of the ramets biomass to different structures (below-ground organs, stems, leaves and flowers) were unchanged with respect to spittlebug density. The only effect of spittlebugs was a 3-4% decrease in ramet height at the end of the growing season.
We argue that the lack of a positive correlation between host-plant preference and larval performance may reflect a constraint on the discriminatory ability of female stem gallers. The damage to goldenrods caused by spittlebugs prior to attack by the stem gallers is similar in effect to potentially innumerable other causes of goldenrod stress (e.g., reduction in ramet growth rates). As a consequence, stem gallers may not be able to discern the subtle differences among stresses that identify which will negatively impact stem-galler offsprings fitness. The fact that goldenrod genotypes differ in their response to stresses would only further complicate the host-selection process. We propose that the stem gallers may have evolved a strategy that uses simple cues as the basis for rejecting similarly stressed plants, whether all of those plant genotype-stress combinations reduce performance or not.