Effects of belowground symbioses, such as those formed with arbuscular mycorrhizal fungi (AMF), can cross the soil surface through plants to have far-reaching effects on aboveground species interactions. By altering nutrient uptake and interacting with plant defensive signaling pathways, AMF may alter plant nutritive and defensive traits. These changes in plant traits may cascade up to affect higher trophic levels, shaping interactions between herbivores and their natural enemies. We manipulated the degree of root colonization by a ubiquitous AMF species (Funneliformis mosseae) to explore interactions between specialist oleander-milkweed aphids (Aphis nerii) and their natural enemies on six North American milkweed species (Asclepias incarnata, A. curassavica, A. syriaca, A. speciosa, A. verticillata, A. sullivantii). In a fully factorial, randomized block field experiment, we counted aphids, predators, and aphid carcasses on all plants for eight weeks from August through September 2015. We hypothesized that aphid colonization, extinction, and predator recruitment would vary among AMF treatments consistently among plant species. Specifically, following the Resource Exchange Model of Plant Defense, we predicted that aphid colonization, predator recruitment, and aphid extinction would be intermediate on plants without AMF, lowest on plants colonized by low amounts of AMF, and greatest on plants highly colonized by AMF.
Results/Conclusions
Aphids were more likely to colonize plants that were colonized by low or high amounts of AMF than to colonize plants lacking AMF. In contrast, aphid extinction was most likely on plants colonized by low amounts of AMF than on those highly colonized or not colonized by AMF. The most common aphid predators, aphid midge flies (Aphidoletes aphidimyza), were differentially attracted to plants colonized by different levels of AMF, with the direction of effects varying among milkweed species. For example, aphid midge flies laid more eggs per aphid on A. curassavica plants not colonized by AMF, A. incarnata and A. syriaca plants colonized by low amounts of AMF, and A. sullivantii plants highly colonized by AMF. Most notably, per capita death rates of aphids from midge flies varied with AMF colonization, such that plants highly colonized with AMF hosted the greatest per capita death rates by aphid midge flies and plants colonized by low amounts of AMF had the least. Our findings are among the first to demonstrate that herbivore population dynamics may be driven not by tritrophic interactions, but by quad-trophic interactions, as AMF alter plant quality to shape the strength of density-dependent predation.