Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

Abstract

Soil biota-plant interactions play a dominant role in terrestrial ecosystems. Through nutrient mineralization and mutualistic or antagonistic interactions with plants soil biota can affect plant performance and physiology and via this affect plant-associated aboveground insects. There is a large body of work in this field that has already been synthesized in various review papers. However, most of the studies have been carried out under highly controlled laboratory or greenhouse conditions. Here, we review studies that manipulate soil organisms of four dominant taxa (i.e. bacteria, fungi, nematodes and soil arthropods) in the field and assess the effects on the growth of plants and interactions with associated aboveground insects. We show that soil organisms play an important role in shaping plant-insect interactions in the field and that general patterns can be found for some taxa. Plant growth-promoting rhizobacteria generally have negative effects on herbivore performance or abundance, most likely through priming of defenses in the host plant. Addition of arbuscular mycorrhizal fungi (AMF) has positive effects on sap sucking herbivores, which is likely due to positive effects of AMF on nutrient levels in the phloem. The majority of AMF effects on chewers were neutral but when present, AMF effects were positive for specialist and negative for generalist chewing herbivores. AMF addition has negative effects on natural enemies in the field, suggesting that AMF may affect plant attractiveness for natural enemies, e.g. through volatile profiles. Alternatively, AMF may affect the quality of prey or host insects mediated by plant quality, which may in turn affect the performance and density of natural enemies. Nematodes negatively affect the performance of sap sucking herbivores (generally through phloem quality) but have no effect on chewing herbivores. For soil arthropods there are no clear patterns yet. We further show that the methodology used plays an important role in influencing the outcomes of field studies. Studies using potted plants in the field and studies that remove target soil taxa by means of pesticides are most likely to detect significant results. Lastly, we discuss suggestions for future research that could increase our understanding of soil biota-plant-insect interactions in the field.