Modulation of plant-mediated interactions between herbivores of different feeding guilds: Effects of parasitism and belowground interactions

Abstract

Herbivory affects subsequent herbivores, mainly regulated by the phytohormones jasmonic (JA) and salicylic acid (SA). Additionally, organisms such as soil microbes belowground or parasitoids that develop inside their herbivorous hosts aboveground, can change plant responses to herbivory. However, it is not yet well known how organisms of trophic levels other than herbivores, below- and above-ground, alter the interactions between insect species sharing a host plant. Here, we investigated whether the parasitoid Aphidius colemani and different soil microbial communities (created through plant-soil feedbacks) affect the JA and SA signalling pathways in response to the aphid Myzus persicae and the thrips Frankliniella occidentalis, as well as subsequent thrips performance. Our results show that the expression of the JA-responsive gene CaPINII in sweet pepper was more suppressed by aphids than by parasitised aphids. However, parasitism did not affect the expression of CaPAL1, a biosynthetic gene of SA. Furthermore, aphid feeding enhanced thrips performance compared with uninfested plants, but this was not observed when aphids were parasitised. Soils where different plant species were previously grown, did not affect plant responses or the interaction between herbivores. Our study shows that members of the third trophic level can modify herbivore interactions by altering plant physiology.

Figure 1

Expression levels of CaPINII in C. annuum in uninfested, aphid-infested, or parasitised aphids- infested plants, each grown in sterile soil, or inoculated with living soil conditioned by the plants A. millefolium or L. perenne. Bars represent mean CaPINII expression levels normalised as 2^−∆∆Ct with standard error bars (n = 4). Bars marked with different letters are significantly different (LSD, P < 0.05), with separate analysis for the two time points (24 and 48 h after aphid infestation).

Figure 2

Expression levels of CaPAL1 in C. annuum in uninfested, aphid-infested, or parasitised aphids- infested plants, each grown in sterile soil, or inoculated with living soil conditioned by the plants A. millefolium or L. perenne. Bars represent mean CaPAL1 expression levels normalised as 2^−∆∆Ct with standard error bars (n = 4). Bars marked with different letters are significantly different (LSD, P < 0.05), with separate analysis for the two time points (24 and 48 h after aphid infestation).

Figure 3

Performance of F. occidentalis, number that reach the adult stage (out of 5 initial individuals) on C. annuum for four different treatments: (a) uninfested plants, (b) aphid-infested plants, (c) parasitised aphid-infested plants, (d) thrips-infested plants, on three different soil types: (a) sterile soil, (b) A. millefolium, (c) L. perenne. Bars represent means ± SE (n = 12 replicates). Different letters indicate significant pairwise differences between infestation treatments (P < 0.05).

Figure 4

Performance of F. occidentalis, length of body size in adult stage for female (A) and male (B) thrips on C. annuum for four different treatments: (a) uninfested plants, (b) aphid infested plants, (c) parasitised aphid infested plants, (d) thrips infested plants, on three different soil types: (a) sterile soil, (b) A. millefolium, (c) L. perenne. Bars represent means ± SE (n = 12). No surviving females were found in thrips infested plants grown on A. millefolium soil. Different letters indicate significant pairwise differences between infestation treatments (P < 0.05).