Oxidation of ingested phenolics in the tree-feeding caterpillar Orgyia leucostigma depends on foliar chemical composition

Tannins are believed to function as antiherbivore defenses, in part, by acting as prooxidants. However, at the high pH found in the midguts of caterpillars, the oxidative activities of different types of tannins vary tremendously: ellagitannins >> galloyl glucoses > condensed tannins. Ingested ascorbate is utilized by caterpillars to minimize phenolic oxidation in the midgut. Thus, leaves that contain higher levels of reactive tannins and lower levels of ascorbate were hypothesized to produce higher levels of phenolic oxidation in caterpillars. We tested this hypothesis with eight species of deciduous trees by measuring their foliar phenolic and ascorbate compositions and measuring the semiquinone radical (oxidized phenolic) levels formed in caterpillars that ingested each species. When the generalist caterpillars of Orgyia leucostigma (Lymantriidae) fed on the leaves of tree species in which condensed tannins were predominant (i.e., Populus tremuloides, P. deltoides, and Ostrya virginiana), semiquinone radical levels were low or entirely absent from the midgut contents. In contrast, species that contained higher levels of ellagitannins (or galloyl rhamnoses; i.e., Quercus alba, Acer rubrum, and A. saccharum) produced the highest levels of semiquinone radicals in O. leucostigma. Low molecular weight phenolics contributed relatively little to the overall oxidative activities of tree leaves compared with reactive tannins. Ascorbate levels were lowest in the species that also contained the highest levels of oxidatively active tannins, potentially exacerbating phenolic oxidation in the gut lumen. We conclude that the tannin compositions of tree leaves largely determine the effectiveness of foliar phenolics as oxidative defenses against caterpillars such as O. leucostigma.