Does This Look Infected? Hidden Host Plant Infection by the Pathogen Botrytis cinerea Alters Interactions between Plants, Aphids and Their Natural Enemies in the Field

Abstract

Few studies have considered whether hidden (asymptomatic) plant pathogen infection alters ecological interactions at the higher trophic levels, even though such infection still affects plant physiology. We explored this question in two field experiments, where two varieties of lettuce (Little Gem, Tom Thumb) infected with Botrytis cinerea were either (1) naturally colonised by aphids or (2) placed in the field with an established aphid colony. We then recorded plant traits and the numbers and species of aphids, their predators, parasitoids and hyperparasitoids. Infection significantly affected plant quality. In the first experiment, symptomatically infected plants had the fewest aphids and natural enemies of aphids. The diversity and abundance of aphids did not differ between asymptomatically infected and uninfected Little Gem plants, but infection affected the aphid assemblage for Tom Thumb plants. Aphids on asymptomatically infected plants were less attractive to predators and parasitoids than those on uninfected plants, while hyperparasitoids were not affected. In the second experiment, when we excluded natural enemies, aphid numbers were lower on asymptomatically and symptomatically infected plants, but when aphid natural enemies were present, this difference was removed, most likely because aphids on uninfected plants attracted more insect natural enemies. This suggests that hidden pathogen infection may have important consequences for multitrophic interactions.