Effects of above- and belowground herbivory of specialists and generalists on the growth and defensive chemicals of introduced and native Chinese tallow seedlings

Abstract

Spatially separated aboveground (AG) and belowground (BG) herbivores can affect each other and alter plant growth and defense, although the outcome of AG-BG herbivore interactions may vary with herbivore type (specialists versus generalists). Here, we explored how AG and BG specialists and generalists interacted on different plant genotypes. We subjected native and introduced seedlings of T. sebifera to herbivory by a specialist/generalist caterpillar, and BG herbivory by a root-knot nematode. We compared interactions between the herbivores and how they influenced the growth and defensive chemicals in T. sebifera. A field survey showed that AG insect exclusion greatly increased the root knot number of nematodes. However, a common-garden experiment showed that the AG specialist only facilitated nematodes on native seedlings, while the AG generalist only facilitated nematodes on introduced plants. The larval biomass of the specialist caterpillar was lower but that of the generalist caterpillar was higher on nematode-infested plants than on uninfested plants. Consistently, laboratory bioassays showed that consumption by the generalist caterpillar increased on nematode-infested plants, but consumption by the specialist caterpillar decreased. The above AG-BG herbivore interactions could be partially explained by changes in tannins and flavonoids. The changes in biomass, tannins and flavonoids after bouts of AG or BG herbivory were dependent on the type of AG caterpillars. Our results demonstrate that herbivore type is important in shaping AG-BG interactions, and highlight the importance of measuring AG and BG linkages to fully understand how plants respond to different groups of herbivores.