Enhanced aphid abundance in spring desynchronizes predator-prey and plant-microorganism interactions.

Climate change leads to phenology shifts of many species. However, not all species shift in parallel, which can desynchronize interspecific interactions. Within trophic cascades, herbivores can be top-down controlled by predators or bottom-up controlled by host plant quality and host symbionts, such as plant-associated micro-organisms. Synchronization of trophic levels is required to prevent insect herbivore (pest) outbreaks. In a common garden experiment, we simulated an earlier arrival time (~2 weeks) of the aphid Rhopalosiphum padi on its host grass Lolium perenne by enhancing the aphid abundance during the colonization period. L. perenne was either uninfected or infected with the endophytic fungus Epichloë festucae var. lolii. The plant symbiotic fungus produces insect deterring alkaloids within the host grass. Throughout the season, we tested the effects of enhanced aphid abundance in spring on aphid predators (top-down) and grass-endophyte (bottom-up) responses. Higher aphid population sizes earlier in the season lead to overall higher aphid abundances, as predator occurrence was independent of aphid abundances on the pots. Nonetheless, after predator occurrence, aphids were controlled within 2 weeks on all pots. Possible bottom-up control of aphids by increased endophyte concentrations occurred time delayed after high herbivore abundances. Endophyte-derived alkaloid concentrations were not significantly affected by enhanced aphid abundance but increased throughout the season. We conclude that phenology shifts in an herbivorous species can desynchronize predator-prey and plant-microorganism interactions and might enhance the probability of pest outbreaks with climate change.