A major challenge in plant-insect interactions is predicting the outcome of multiple herbivory, which can have drastically different effects on plants and their respective communities compared to simple additive effects. This can be especially difficult for interactions between herbivores above and belowground, which never interact directly but create a very different host environment for subsequent feeders through changes to plant nutrition and chemistry. Thus far, the variation in outcomes has made it difficult to predict how a given set of species will interact unless that combination has been previously studied; furthermore, it is often unclear how these interactions change when exposed to a wider community. We conducted a meta-analysis along with greenhouse and laboratory experiments to determine how plant-mediated interactions between above- and belowground herbivores change under a suite of biologically relevant factors. First, we determined what the overall outcomes were for interactions between aboveground insect herbivores and belowground plant feeding nematodes, and how these interactions affected chewing insect growth, phloem-feeding insect reproduction, and nematode reproduction, as well as carbon and nitrogen location within a plant. Second, we used laboratory and greenhouse experiments to investigate how constitutive plant defense altered the plant-mediated interaction between a chewing herbivore (Colorado potato beetle, Leptinotarsa decemlineata) and the Northern root-knot nematode (Meloidogyne hapla). Finally, we investigated how belowground damage by the Western corn rootworm (Diabrotica virgifera virgifera) influenced population growth of corn aphids (Rhopalosiphum maidis) as well as the preference and performance of a generalist lady beetle (Hippodamia convergens) and an aphid parasitoid (Aphidius colemani), as well as aboveground plant volatiles. We found that foliar chewing insect growth was decreased in the presence of gall nematodes and increased in the presence of cyst nematodes, and that concurrent feeding by plant feeding nematodes and aboveground insect herbivores alters the distribution of carbon and nitrogen in the plant. Next, we found that constitutive level of plant defense can alter the directionality and strength of interactions between nematodes and foliar chewing herbivores. Lastly, we determined that feeding by a belowground chewing herbivore can indirectly affect foliar aphid reproduction as well as the third trophic level through reproductive effects on aphids and aboveground plant volatiles, but that these effects are change over time and affect a predator and parasitoid differently. This work fills in several gaps in our existing framework of plant-mediated interactions and allows us to fine-tune predictions about which focal systems will be most susceptible to plant-mediated effects, and what plant or insect traits will dampen effects or promote cascading population changes.
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