Abstract

Plants interact with a variety of other community members that have the potential to indirectly influence each other through a shared host plant. Arbuscular mycorrhizal fungi (AMF) are generally considered plant mutualists because of their generally positive effects on plant nutrient status and growth. AMF may also have important indirect effects on plants by altering interactions with other community members. By influencing plant traits, AMF can modify aboveground interactions with both mutualists, such as pollinators, and antagonists, such as herbivores. Because herbivory and pollination can dramatically influence plant fitness, comprehensive assessment of plant–AMF interactions should include these indirect effects. To determine how AMF affect plant–insect interactions, we grew Cucumis sativus (Cucurbitaceae) under five AMF inoculum treatments and control. We measured plant growth, floral production, flower size, and foliar nutrient content of half the plants, and transferred the other half to a field setting to measure pollinator and herbivore preference of wild insects. Mycorrhizal treatment had no effect on plant biomass or floral traits but significantly affected leaf nutrients, pollinator behavior, and herbivore attack. Although total pollinator visitation did not vary with AMF treatment, pollinators exhibited taxon-specific responses, with honey bees, bumble bees, and Lepidoptera all responding differently to AMF treatments. Flower number and size were unaffected by treatments, suggesting that differences in pollinator preference were driven by other floral traits. Mycorrhizae influenced leaf K and Na, but these differences in leaf nutrients did not correspond to variation in herbivore attack. Overall, we found that AMF indirectly influence both antagonistic and mutualistic insects, but impacts depend on the identity of both the fungal partner and the interacting insect, underscoring the context-dependency of plant–AMF interactions.

Highlights

  • Plants interact with a variety of organisms both above and below the soil surface

  • The outcomes of plant–arbuscular mycorrhizal fungi (AMF) interactions have historically focused on the direct effects of the fungi on plants, such as plant growth or nutrient content

  • Plant growth and fitness are influenced by community members, whose interactions may be modified by AMF-driven changes in plant traits

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Summary

Introduction

Plants interact with a variety of organisms both above and below the soil surface. Belowground interactions between plants and other organisms influence, and are influenced by, interactions aboveground (Bardgett and Wardle, 2003; Wardle et al, 2004; van der Putten et al, 2009). Among the most abundant and widespread soil microbes are arbuscular mycorrhizal fungi (AMF), members of the phylum Glomeromycota that form associations with plant roots and exchange nutrients, such as phosphorus and nitrogen, for plant-derived carbon (Smith and Read, 2008). These globally important fungi interact with 60–80% of terrestrial plant species (Smith and Smith, 2011) and generally confer growth and fitness benefits (Smith and Read, 2008). The direct effects of AMF on plants may alter plant traits that mediate interactions between plants and insects, such as pollinators or herbivores, with important consequences for plant fitness (Wolfe et al, 2005; Koricheva et al, 2009; Vannette and Rasmann, 2012)

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