Plant-soil microbiota-herbivore interactions can play a pivotal role in plant community dynamics. Plants can influence soil microbiota through secretion of root exudates, antibiotics, and signaling molecules. Soil microbiota, in turn, can positively impact plants through the provision of nutrients, growth hormones, or protection against plant pathogens, or negatively impact them via infection by pathogenic microbes. Meanwhile, herbivory can influence the quantity and quality of root exudation, with subsequent positive or negative feedbacks to the plant and the soil microbiota. If non-native invasive plants benefit from interactions with soil microbiota, while native plants suffer from changes in the soil induced by invasives and herbivores, then this may be a mechanism for non-native plant success. Our objective was to investigate the roles of soil microbiota and root herbivory in reduced native plant recruitment that frequently follows leafy spurge (Euphorbia esula) infestations in the Great Plains, USA. In factorial greenhouse experiments, leafy spurge was grown in sterilized soils inoculated with field soil and subjected to herbivory from two flea beetle species (Aphthona lacertosa and A. nigriscutis). The leafy spurge was subsequently removed and soils were sown with seeds of eight native grassland plants to quantify rates of germination and survivorship.

Results/Conclusions

In the absence of leafy spurge, germination rates were lower in sterilized soils than in inoculated soils for 7 of the 8 species, although the differences were not significant. Leafy spurge presence significantly reduced subsequent germination rates of Artemisia frigida, a trend that four other species followed. Flea beetle effects varied among native plant species. Aphthona lacertosa reduced germination and survival of A. frigida in sterilized but not inoculated soils, while A. nigriscutis increased germination of Aster ericoides in both sterilized and inoculated soils. Germination rates of all species decreased with increasing numbers of A. lacertosa beetles. These results indicate that leafy spurge alters soil conditions, either through changes in soil microbiota or through persistent root exudates, in ways that are detrimental to germination and establishment of some native plants. The higher germination rates in inoculated soils suggests that native soil microbiota are beneficial to native plant establishment. The influence of flea beetles is species-specific, with A. lacertosa reducing, and A. nigriscutis increasing, germination rates of some plant species. While the specific mechanisms behind these results are unknown, it is clear that invasive species-soil microbiota-herbivore species interactions can influence native plant establishment.