Herbivorous insect decreases plant nutrient uptake: the role of soil nutrient availability and association of below‐ground symbionts

1. Plants take nutrients from the rhizosphere via two pathways: (i) by absorbing soil nutrients directly via their roots and (ii) indirectly via symbiotic associations with nutrient‐providing microbes. Herbivorous insects can alter these pathways by herbivory, adding their excrement to the soil, and affecting plant–microbe associations. 2. Little is known, however, about the effects of herbivorous insects on plant nutrient uptake. Greenhouse experiments with soybean, aphids, and rhizobia were carried out to examine the effects of aphids on plant nutrient uptake. 3. First, the inorganic soil nitrogen and the sugar in aphid honeydew between aphid‐infected and ‐free plants were compared. It was found that aphid honeydew added 41 g m^?2 of sugar to the soil, and that aphids decreased the inorganic soil nitrogen by 86%. This decrease may have been caused by microbial immobilisation of soil nitrogen followed by increased microbial abundance as a result of aphid honeydew. 4. Second, nitrogen forms in xylem sap between aphid‐infected and ‐free plants were compared to examine nitrogen uptake. Aphids decreased the nitrogen uptake via both pathways, and strength of the impact on direct uptake via plant roots was greater than indirect uptake via rhizobia. The reduced nitrogen uptake by the direct pathway was as a result of microbial immobilisation, and that by the indirect pathway was probably because of the interaction of microbial immobilisation and carbon stress, which was caused by aphid infection. 5. The present results demonstrate that herbivorous insects can negatively influence the two pathways of plant nutrient uptake and alter their relative importance.