How slug herbivory of hybrid willows alters chemistry, growth, and susceptibility to diverse plant enemies

Background/Question/Methods

Herbivores often cause extensive seedling mortality and non-random attack can alter the genetic architecture of the resulting population and have cascading effects on other consumers. We tested the hypothesis that herbivory by the exotic slug, Arion subfuscus, leads to non-random survival of hybrid willow seedlings (favors those that are well-defended and less nutritious). We further examined whether selection by slugs altered the subsequent susceptibility of plants to other phytophages. We used F₂ hybrids for two reasons. First, hybridization generates broad variation in traits that can be selected for or against, and second, non-random survival of hybrids has the potential to alter patterns of introgression. We created two populations of F₂ hybrid willows, an unattacked control and an attacked (=selected) population. We then quantified the concentrations of defensive (tannins and phenolic glycosides) and nutritional (nitrogen and protein) chemicals and performed a series of experiments evaluating the susceptibility of these two populations to slugs and others phytophages. 

Results/Conclusions

Selection by Arion subfuscus did not, as expected, lead to an increase in phenolic glycoside or tannin concentrations in the attacked population. Rather these plants had higher foliar nitrogen and protein, a lower carbon to nitrogen ratio than control plants, and greater above ground biomass. The resulting population also differed in susceptibility to their enemies.  As expected plants that survived the initial attack were less palatable to slugs in subsequent assays. More interestingly, selection caused greater susceptibility to a native beetle (Chrysomela knabi), an exotic beetle (Plagiodera versicolora), and an indigenous pathogen (Melampsora epitea). This suggests that resistance to slugs involved a tradeoff in resistance to these three phytophages. Overall these results demonstrate that selection for resistance to one species may increase susceptibility to other species. Moreover, our findings suggest that exotic herbivore species may have direct and indirect effects that have been underappreciated. Our results also indicate that resistance evolution to one herbivore may give rise to greater susceptibility to other enemies and shape the introgression of an adaptive trait.