Bottom-up effects of glucosinolate variation on aphid colony dynamics in wild cabbage populations

1. There is an ongoing debate about the relative importance of top-down and bottom-up regulation of herbivore dynamics in the wild. Secondary metabolites, produced by plants, have negative effects on survival and growth of some herbivore species, causing bottom-up regulation of population dynamics. Herbivore natural enemies may use plant secondary metabolites as cues to find their prey, but their survival and reproduction can also be influenced by the upward cascade of secondary metabolites through the food web. Thus plant chemistry might also affect herbivore populations by mediating top-down regulation. 2. We investigated the influence of heritable variation in aliphatic glucosinolates, a class of secondary metabolites produced by Brassica plants, on the relative importance of top-down and bottom-up regulation of Brevicoryne brassicae (mealy cabbage aphid) colonies in natural Brassica oleracea (wild cabbage) populations. We manipulated natural enemy pressure on plants differing in their glucosinolate profiles, and monitored aphid colony growth and disperser production. 3. Aphid colony sizes were significantly smaller on plants producing sinigrin, compared with plants producing alternative aliphatic glucosinolates. Aphid natural enemy numbers correlated with aphid colony size, but there was no additional effect of the plants' chemical phenotype on natural enemy abundance. Furthermore, experimental reduction of natural enemy pressure had no effect on aphid colony size or production of winged dispersers. 4. Our results provide evidence for glucosinolate-mediated, bottom-up regulation of mealy cabbage aphid colonies in natural populations, but we found no indication of top-down regulation. We emphasise that more studies of these processes should focus on tritrophic interactions in the wild.