Density-dependent dynamics of plant defense through three trophic levels: milkweed, aphids and coccinellids

Plant chemical defenses that are sequestered by aposematic insect herbivores present a problem for plants that may be resolved at the third trophic level by natural enemies. It has been shown that a neotropical milkweed reduced “source” cardenolide expression when the density of an aposematic aphid was low and then induced cardenolide expression as the density increased. We tested the hypothesis that such “U-shaped” cardenolide expression in response to changing herbivore density should impact both aphid defense and the functional response of an aphidophagous predator. We manipulated the density of the aposematic oleander aphid, Aphis nerii on the neotropical milkweed, Asclepias curassavica, to determine whether plant cardenolides change in response to phloem-feeding aphids as well as sequestration of these steroidal defenses by the aphids at different densities. Aphids from varying density plants were fed to newly emerged, 4th instar larvae of Coccinella sepempunctata to measure their functional response to aphid density. Our results show that both milkweeds and aphids had high cardenolide concentrations at low and high aphid densities, but cardenolide concentrations were low in intermediate density plants and their aphids. This “U-shaped” cardenolide response impacted natural enemies, which generated a domed, or type-4 functional response feeding on A. nerii and an overall depression of the type 4 functional response in comparison with the type 2 response generated by palatable, control aphids. We further hypothesize that this response to aposematic prey will destabilize the dynamics of such tritrophic interactions and is a possible resolution of the lethal plant defense paradox.