Aphid honeydew reduces soil nitrogen and increases host plant growth

Plants are known to affect their soils in ways that can have positive or negative effects on themselves and other plants, often described as plant-soil feedbacks. However, less is known about the potential for herbivores to change the soil in ways that affect plant growth. Many sap-feeding insect herbivores produce a sugary secretion called honeydew. Here, we ask if seasonal pulses of accumulated aphid (Aphis nerii) honeydew reduce the availability of soil nitrogen below milkweed (Asclepias fascicularis) host plants, and how honeydew-conditioned soil affects the relative seedling growth of host plants and other, potentially competing plant species. We hypothesized that: (1) honeydew would reduce plant-available nitrogen in the soil, reflecting the expectation for increased microbial immobilization in response to high carbon inputs, and (2) reduced nitrogen availability would have a greater negative effect on the growth of cheatgrass (Bromus tectorum) and yellow star-thistle (Centaurea solstitialis) than milkweed, reflecting the expectation of greater nitrogen limitation in disturbance-adapted, non-native, annual plant species compared with native, perennial plants. We found that the addition of honeydew at accumulated levels reduced total inorganic soil nitrogen by 48.8% relative to controls. Unexpectedly, milkweed seedlings were 90% taller and had 4.2 times greater dry biomass in honeydew-conditioned soil than in the control group, but we did not observe any effects on the growth of cheatgrass (Bromus tectorum) and yellow star-thistle (Centaurea solstitialis) seedlings. These results suggest the possibility of a positive plant-herbivore-soil feedback for milkweeds, mediated by aphid honeydew.