Feeding specialization shapes the bottom‐up effect of arbuscular mycorrhizal fungi across a plant–aphid–parasitoid system

Abstract

Societal Impact StatementArbuscular mycorrhizal fungi (AMF) impact the relationships between plants, aphids (insects that feed on plant phloem), and their natural enemies (insects that prey on or parasitize aphids). The presence of AMF influences the growth and population of different aphid species and affects the development of aphid‐killing wasps and their attraction to plants. This research has been conducted also considering the insects' feeding strategy and their feeding specialization. This study provides novel perspectives on how these fungi shape interactions in the natural world, offering potential insights for the development of sustainable pest management strategies in agriculture.Summary Arbuscular mycorrhizal fungi (AMF) are major root symbionts regulating plant physiology. Their presence affects the performance of aboveground insect herbivores in relation to their feeding strategy and their feeding specialization. For example, the effect of the arbuscular mycorrhizal (AM) symbiosis on chewing insects, positive for specialists and negative for generalists, has been previously demonstrated. Conversely, the impact of AMF on phloem‐suckers with relatively different levels of specialization remains unexplored. We tested the influence of the AM Funneliformis mosseae on the fitness of the specialist aphid Acyrthosiphon pisum and the generalist aphid Myzus persicae on Vicia faba plants. Further, we investigated the effects of AMF on the higher trophic level, the aphid parasitoids Aphidius ervi (specialist) and Aphidius colemani (generalist), by evaluating plant attractiveness and parasitoid fitness. To support the results of behavioral and biological bioassays we characterized the photosynthetic parameters, the volatilome and the transcriptome of tested plants. Mycorrhizal plants proved unsuitable for the generalist M. persicae but enhanced the fitness of the specialist A. pisum. The AM symbiosis had no effects on the behavioral response of A. colemani and enhanced the attraction and fitness of A. ervi. Volatilome and transcriptome profiling corroborated the results of bioassay highlighting a bottom‐up effect of the AMF across a plant–aphid–parasitoid system.