Context-dependency of arbuscular mycorrhizal fungi on plant-insect interactions in an agroecosystem

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.

Keywords: Cucumis sativus; aboveground–belowground; arbuscular mycorrhizal fungi; herbivore; indirect interaction; pollinator.

FIGURE 1

Effects of AMF inoculation treatments on percent AMF colonization. Values are fitted means ± 1 SE.

FIGURE 2

Effects of AMF inoculation treatments on (A) leaf Na content and (B) leaf K content. Values are fitted means expressed in parts per million ± 1 SE for Na and parts per thousand ± 1 SE for K. Asterisk indicates significant difference from non-mycorrhizal control.

FIGURE 3

Effects of AMF inoculation treatments on (A) bumble bee visits per plant, (B) Lepidoptera visits per plant, (C) honey bee probes per flower, and (D) Lepidoptera probes per flower. Values are fitted means ± 1 SE. Asterisks indicates significant differences based on a priori contrasts between non-mycorrhizal control and each single species inoculum (G. clarum, G. custos, R. irregularis, and commercial). Double dagger indicates significant difference based on a priori contrast between the mixed inoculum and its component single-species inocula.

FIGURE 4

Effects of AMF inoculation treatments on probability of herbivore attack. Values are fitted means ± 1 SE, transformed from logits to probability for ease of interpretation.