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.

Keywords: aphid; asymptomatic infection; multitrophic interaction; parasitoid; plant disease; predatory insect.

Figure 1

Influence of the lettuce infection status (uninfected/symptomatic/asymptomatic) and variety on the mean (+/−SE) number of (a) aphids, (b) parasitoid mummies and (c) predators found on plants in the sentinel experiment. Treatments sharing the same letters above each bar are not significantly different at p < 0.05 following post hoc tests.

Figure 2

Network analysis of species found on lettuce in the sentinel experiment. Link widths represent the observed frequency of interactions, with red links being stronger and blue links being weaker than expected compared to the null model. The white links represent no significant differences. Bar widths at the two levels indicate the relative abundances of species at different trophic levels for lettuce and (a) aphids (AF, Aphis fabae; AL, Acyrthosiphon lactucae; ME, Macrosiphum euphorbiae; MO, Myzus ornatus; MP, Myzus persicae); (b) parasitoids (AE, Aphidius ervi; AM, Aphidius matricariae; AV, Asaphes vulgaris; AX, Alloxysta victrix; DC, Dendrocerus carpenteri; DR, Diaeretiella rapae; PG, Praon gallicum); and (c) predators (AS, Anthocoris nemorum; CS, Coccinella septempunctata; EB, Episyrphus balteatus; HA, Harmonia axyridis; LL, lacewing; PQ, Propylea quatuordecimpunctata; SR, Syrphus ribesii; TS, Tachyporus sp.). Abbreviations—U: uninfected plants; A: asymptomatic infected plants; S: symptomatic infected plants; LG: Little Gem variety; TT: Tom Thumb variety.

Figure 3

Influence of the infection status (uninfected/symptomatic/asymptomatic) and plant variety on the mean (+/−SE) number of aphids on lettuce plants per recording day in the established aphid colony experiment. Aphids recorded on plants where protected from (a,b) or exposed to aphid natural enemies (c,d). Abbreviations—U: uninfected plants; A: asymptomatic infected plants; S: symptomatic infected plants; LG: Little Gem variety; TT: Tom Thumb variety.

Figure 4

Influence of the lettuce infection status (uninfected/symptomatic/asymptomatic) and variety on the mean (+/−SE) number of (a) parasitoid mummies and (b) predators found on plants in the established aphid colony experiment. Treatments sharing the same letters above each bar are not significantly different at p < 0.05 following post hoc tests.

Figure 5

Network analysis of species found on lettuce in the established aphid colony experiment. Link widths represent the observed frequency of interactions, with red links being stronger and blue links being weaker than expected compared to the null model. The white links represent no significant differences. Bar widths at the two levels indicate the relative abundances of species at different trophic levels for lettuce and (a) parasitoids (AE: Aphidius ervi; AM: Aphidius matricariae; AV: Asaphes vulgaris; DR: Diaeretiella rapae; PG: Praon gallicum) and (b) predators (AB: Adalia bipunctata: CS: Coccinella septempunctata; EB: Episyrphus balteatus; HA: Harmonia axyridis; SR: Syrphus ribesii). Abbreviations—U: uninfected plants; A: asymptomatic infected plants; S: symptomatic infected plants; LG: Little Gem variety; TT: Tom Thumb variety.