Above-ground herbivory by red milkweed beetles facilitates above- and below-ground conspecific insects and reduces fruit production in common milkweed

1. Initial herbivory and induced plant responses can influence subsequent above- and below-ground herbivore attack. When two life stages of the same herbivore damage different plant parts sequentially, there is strong potential for plants to respond with induced plant defence against the later attacker. Alternatively, the earlier attacker could manipulate the host plant to facilitate the later-feeding life stage. 2. We studied herbivory by foliage-feeding adults and root-feeding larvae of the red milkweed beetle (Tetraopes tetraophthalmus) on native common milkweed (Asclepias syriaca) in laboratory and field experiments. We applied factorial above- and below-ground herbivory treatments to test for induced responses, effects on later-feeding conspecific larvae, and damage by naturally colonizing herbivores, including adult T. tetraophthalmus. 3. We found that the inducibility of toxic cardenolides was systemic across the root-shoot barrier, with the highest concentrations in plants damaged both above- and below-ground. Initial above-ground herbivory increased root damage and larval survival, suggesting an increase in root quality following leaf herbivory. Initial below-ground herbivory did not affect the performance of later-feeding larvae, indicating limited importance of induced root cardenolides and competition between clutches of T. tetraophthalmus. 4. In a natural milkweed population, initial above-ground herbivory attracted conspecific adults and milkweed leaf beetles (Labidomera clivicollis) and ultimately reduced fruit production by 33%. Nonetheless, the probability of damage by monarch caterpillars (Danaus plexippus) was reduced on plants initially damaged by T. tetraophthalmus above-ground, likely due to reduced oviposition following induced plant responses. 5. Synthesis. Induced plant responses of common milkweed to above-ground damage by adult T. tetraophthalmus both facilitate further damage by adults and enhance the performance of their root-feeding larvae, most likely as a result of host plant manipulation. Although the same induction reduced monarch herbivory, the net effect of these interactions was negative for the plant as fruit production was substantially reduced. These results imply that host plant manipulation may be especially common by specialist herbivores that have sequential above- and below-ground life stages.