Herbivore-driven disruption of arbuscular mycorrhizal carbon-for-nutrient exchange is ameliorated by neighboring plants

Abstract

Arbuscular mycorrhizal fungi colonize the roots of most plants, forming a near-ubiquitous symbiosis¹ that is typically characterized by the bi-directional exchange of fungal-acquired nutrients for plant-fixed carbon.² Mycorrhizal fungi can form below-ground networks^3,4,5,6 with potential to facilitate the movement of carbon, nutrients, and defense signals across plant communities.^7,8,9 The importance of neighbors in mediating carbon-for-nutrient exchange between mycorrhizal fungi and their plant hosts remains equivocal, particularly when other competing pressures for plant resources are present. We manipulated carbon source and sink strengths of neighboring pairs of host plants through exposure to aphids and tracked the movement of carbon and nutrients through mycorrhizal fungal networks with isotope tracers. When carbon sink strengths of both neighboring plants were increased by aphid herbivory, plant carbon supply to extraradical mycorrhizal fungal hyphae was reduced, but mycorrhizal phosphorus supply to both plants was maintained, albeit variably, across treatments. However, when the sink strength of only one plant in a pair was increased, carbon supply to mycorrhizal fungi was restored. Our results show that loss of carbon inputs into mycorrhizal fungal hyphae from one plant may be ameliorated through inputs of a neighbor, demonstrating the responsiveness and resilience of mycorrhizal plant communities to biological stressors. Furthermore, our results indicate that mycorrhizal nutrient exchange dynamics are better understood as community-wide interactions between multiple players rather than as strict exchanges between individual plants and their symbionts, suggesting that mycorrhizal C-for-nutrient exchange is likely based more on unequal terms of trade than the "fair trade" model for symbiosis.

Keywords: aphids; arbuscular mycorrhiza; carbon; herbivory; mycorrhiza; mycorrhizal networks; nutrient exchange; nutrients; plant communities; symbiosis.