Metabolism or behavior: explaining the performance of aphids on alkaloid-producing fungal endophytes in annual ryegrass (Lolium multiflorum).

Plant-herbivore interactions are often mediated by plant microorganisms, and the "defensive mutualism" of epichloid fungal endophytes of grasses is an example. These endophytes synthesize bioactive alkaloids that generally have detrimental effects on the performance of insect herbivores, but the underlying mechanisms are not well understood. Our objective was to determine whether changes in the physiology and/or behavior of aphids explain the changes in performance of insects feeding on endophytic plants. We studied the interaction between the aphid Rhopalosiphum padi and the annual ryegrass Lolium multiflorum symbiotic (E+) or not symbiotic (E-) with the fungus Epichloë occultans that can synthesize loline alkaloids. We hypothesized that aphids feeding on E+ plants have higher energetic demands for detoxification of fungal alkaloids, thereby negatively impacting the individual performance, population growth, and structure. Aphids growing on E+ plants had lower values in morphometric and functional variables of individual performance, displayed lower birth rate, smaller population size, and dramatic structural changes. However, aphids exhibited lower values of standard metabolic rate (SMR) on E+ plants, which suggests no high costs of detoxification. Behavioral variables during the first 8 h of feeding showed that aphids did not change the phloem sap ingestion with the presence of fungal endophytes. We hypothesize that aphids may maintain phloem sap ingestion according to their fungal alkaloid tolerance capacity. In other words, when alkaloid concentrations overcome tolerance threshold, ingestion of phloem should decrease, which may explain the observed lower values of SMR in E+ feeding aphids.

Symbiotic fungal endophytes control insect host-parasite interaction webs.

Symbiotic microorganisms that live intimately associated with terrestrial plants affect both the quantity and quality of resources, and thus the energy supply to consumer populations at higher levels in the food chain. Empirical evidence on resource limitation of food webs points to primary productivity as a major determinant of consumer abundance and trophic structure. Prey quality plays a critical role in community regulation. Plants infected by endophytic fungi are known to be chemically protected against herbivore consumption. However, the influence of this microbe-plant association on multi-trophic interactions remains largely unexplored. Here we present the effects of fungal endophytes on insect food webs that reflect limited energy transfer to consumers as a result of low plant quality, rather than low productivity. Herbivore-parasite webs on endophyte-free grasses show enhanced insect abundance at alternate trophic levels, higher rates of parasitism, and increased dominance by a few trophic links. These results mirror predicted effects of increased productivity on food-web dynamics. Thus 'hidden' microbial symbionts can have community-wide impacts on the pattern and strength of resource-consumer interactions.