BackgroundThe average nitrogen-to-phosphorus ratio (N∶P) of insect herbivores is less than that of leaves, suggesting that P may mediate plant-insect interactions more often than appreciated. We investigated whether succession-related heterogeneity in N and P stoichiometry influences herbivore performance on N-fixing lupin (Lupinus lepidus) colonizing primary successional volcanic surfaces, where the abundances of several specialist lepidopteran herbivores are inversely related to lupin density and are known to alter lupin colonization dynamics. We examined larval performance in response to leaf nutritional characteristics using gelechiid and pyralid leaf-tiers, and a noctuid leaf-cutter.Methodology/Principal FindingsWe conducted four studies. First, growth of larvae raised on wild-collected leaves responded positively to leaf %P and negatively to leaf carbon (%C), but there was no effect of %N or quinolizidine alkaloids (QAs). Noctuid survival was also positively related to %P. Second, we raised gelechiid larvae on greenhouse-grown lupins with factorial manipulation of competitors and soil N and P. In the presence of competition, larval mass was highest at intermediate leaf N∶P and high %P. Third, survival of gelechiid larvae placed on lupins in high-density patches was greater when plant competitors were removed than on controls. Fourth, surveys of field-collected leaves in 2000, 2002, and 2003 indicated that both %P and %N were generally greater in plants from low-density areas. QAs in plants from low-density areas were equal to or higher than QAs in high-density areas.Conclusions/SignificanceOur results demonstrate that declines in lupin P content under competitive conditions are associated with decreased larval growth and survival sufficient to cause the observed negative relationship between herbivore abundance and host density. The results support the theoretical finding that declines in stoichiometric resource quality (caused here by succession) have the potential to cause a decrease in consumer abundance despite very dense quantities of the resource.