Soil arthropod communities collected from agricultural soils influence wheat growth and modify phytohormone responses to aboveground herbivory in a microcosm experiment

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Soil arthropods can affect plant growth and aboveground interactions directly via root herbivory and indirectly through nutrient cycling and interactions with soil microorganisms. Research on these effects of soil arthropods has focused on a few taxa within natural systems, largely neglecting agroecosystems and arthropod community-level effects. This study investigated the effects of soil arthropod communities from cereal-based agroecosystems on wheat plant growth and above-belowground interactions. Nutrient cycling and wheat growth were measured in a greenhouse microcosm experiment using field-collected agricultural soils from two rotational schemes with and without their soil arthropod communities. The effects of soil arthropods on aboveground phytohormones and colony growth of an aphid [Metopolophium festucae cerealium (Stroyan)] infesting the plants were measured. Wheat grown in soils with arthropod communities had significantly greater root (+ Arth mean: 0.15 ± 0.01 g; − Arth mean: 0.06 ± 0.01 g; F1,54 = 72.34, p < 0.001) and shoot biomass (+ Arth mean: 0.39 ± 0.03 g; − Arth mean: 0.24 ± 0.03 g; F1,54 = 17.61, p < 0.001), greater soil nitrate concentrations (+ Arth mean: 62.18 ± 4.76 mg NO3− - N kg−1 soil; − Arth mean: 13.06 ± 0.61 mg NO3− - N kg−1 soil; F1,54 = 99.89, p < 0.001), and altered root architecture compared to controls. Soil arthropod communities collected from the two rotational schemes differed significantly in abundance and diversity, but affected wheat growth similarly. Aphid colony growth (+ Arth mean: 30.50 ± 4.06; − Arth mean: 22.13 ± 3.36; χ21,27 = 21.19, p < 0.001), but not plant damage by aphids (+ Arth mean: 2.72 ± 0.17, − Arth mean: 2.69 ± 0.16; F1,27 = 0.02, p > 0.05), was significantly greater on wheat grown in soils with arthropods. Aphids, in turn, modified the effects of soil arthropods on root architecture and increased the abundance of soil arthropods. Wheat grown in soils with arthropods had increased levels of stress- and defense-related phytohormones in response to aphid herbivory, while phytohormones of wheat plants grown in soils without arthropods did not differ with aphid presence. Soil arthropod communities may help plants defend against herbivores aboveground by facilitating phytohormone induction while offsetting costs by increasing soil nutrients and modifying plant growth. By using taxonomically diverse field-collected soil arthropod communities from agroecosystems, this study showed that community-level effects on plant growth are more complex and dynamic than the effects of any single taxon, such as Collembola, illustrating that interactions within communities can produce emergent properties that alter the net effect of soil arthropods on plant growth. The results indicate that community-level effects of soil organisms should be considered as part of sustainable plant production and protection strategies.