Insect herbivory but not plant pathogen infection drive floral volatile-mediated indirect effects on pollinators and plant fitness in Brassica rapa

Samenvatting

Plant enemies can indirectly affect pollinators by modifying plant traits, but simultaneous tests of herbivore and pathogen effects are lacking, and the role of floral volatiles has seldom been assessed. In this study, we tested for indirect effects of insect herbivores and pathogens on pollinator attraction via altered floral volatile emissions, and its consequences for plant fitness in Brassica rapa. Plants in the field were exposed to either no damage or damage by caterpillars (Mamestra brassicae), aphids (Brevicoryne brassicae), a leaf fungus (Sclerotinia sclerotiorum), or a bacterium (Xanthomonas campestris pv. campestris). We then recorded pollinator visits and measured floral traits (flower number, volatiles) and plant fitness-correlates. We additionally performed a greenhouse experiment with artificial floral emitters to test for effects of target volatiles on pollinator attraction. In the field experiments, relative to controls, plants subjected to herbivory by the aphid B. brassicae (but not those exposed to the other enemies) exhibited a marked reduction in the emission of two volatile organic compounds (nonanal and 2-butyl-1-octanol), experienced lower pollinator visits and produced seeds of lower quality in terms of seed biomass and germination rate, while flower output itself was not affected. Consistently, artificial emitters with reduced amounts of these volatile organic compounds were less attractive to pollinators under greenhouse conditions. Synthesis. These results provide strong evidence for volatile-mediated indirect interactions between plant enemies and pollinators ultimately impacting plant fitness, and further point at enemy and compound specificity in such effects.