Abstract
Herbivore suppression is mediated by both plant defenses and predators. In turn, plant defenses are impacted by soil fertility and interactions with soil bacteria. Measuring the relative importance of nutritional and microbial drivers of herbivore resistance has proven problematic, in part because it is difficult to manipulate soil-bacterial community composition. Here, we exploit variation in soil fertility and microbial biodiversity across 20 farms to untangle suppression of aphids (Brevicoryne brassicae) through bottom–up and top–down channels. We planted Brassica oleracea plants in soil from each farm, manipulated single and dual infestations of aphids alone or with caterpillars (Pieris rapae), and exposed aphids to parasitoid wasps (Diaeretiella rapae) in the open field. We then used multi-model inference to identify the strongest soil-based predictors of herbivore growth and parasitism. We found that densities of Bacillus spp., a genus known to include plant-growth-promoting rhizobacteria, negatively correlated with aphid suppression by specialist parasitoids. Aphid parasitism also was disrupted on plants that had caterpillar damage, compared to plants attacked only by aphids. Relative abundance of Pseudomonas spp. bacteria correlated with higher aphid growth, although this appeared to be a direct effect, as aphid parasitism was not associated with this group of bacteria. Non-pathogenic soil bacteria are often shown to deliver benefits to plants, improving plant nutrition and the deployment of anti-herbivore defenses. However, our results suggest that these plant growth-promoting bacteria may also indirectly weaken top–down aphid suppression by parasitoids and directly improve aphid performance. Against a background of varying soil fertility, microbial biodiversity, competing herbivores, and natural enemies, we found that effects of non-pathogenic soil microbes on aphid growth outweighed those of nutritional factors. Therefore, predictions about the strength of plant defenses along resource gradients must be expanded to include microbial associates.
Highlights
Chemical defenses induced by plants in response to herbivore attack often trade-off with plant growth due to resource allocation costs, genetic costs, and opportunity costs of prioritizing defense-associated physiological processes over growth (Züst and Agrawal, 2017)
Caterpillars (P. rapae) used in our experiments came from a lab colony, and aphids (B. brassicae) came from a wild colony collected from a single kale plant (Brassica oleracea var. acephala) on April 12, 2016
We identified known plant-growth-promoting rhizobacteria (PGPR) P. fluorescens at the species level, while the majority of other Pseudomonas amplicon sequence variants (ASVs) failed to match beyond the genus level
Summary
Chemical defenses induced by plants in response to herbivore attack often trade-off with plant growth due to resource allocation costs, genetic costs, and opportunity costs of prioritizing defense-associated physiological processes over growth (Züst and Agrawal, 2017). Tritrophic Interactions Over Soil Gradients investments in defense diminish under high nutrient conditions (Coley et al, 1985; Herms and Mattson, 1992). Defense induction is governed by herbivore community composition (Stam et al, 2014) and microbial associates of host plants (Pineda et al, 2017), among numerous other ecological factors. Production of secondary metabolites induced by chewing herbivores can be constrained when chewers and suckers co-occur, due to antagonism between defense signaling pathways (Thaler et al, 2012), while plant-growth-promoting rhizobacteria (PGPR) can prime inducible defenses in advance of herbivory (Pineda et al, 2010). Complex interactions between soil microbes, plants, herbivores, and natural enemies suggest that simple predictions made about defense investments along resource gradients are inadequate, but the importance of each of these numerous drivers of herbivore defense remain unclear
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