Nitrogen deficiency affects bottom-up cascade without disrupting indirect plant defense

Nitrogen (N) is an important macronutrient for plants and insects alike, and the availability of this critical element may considerably modify bottom-up effects in tritrophic systems. By using hydroponically cultured Glycine max, we investigated the impact of N deficiency on plant growth, photosynthetic efficiency, primary metabolism, and herbivore-induced volatile (VOC) emission. Cascading effects of N deficiency on higher trophic levels were assessed by measuring the performances of the herbivore Spodoptera frugiperda and its parasitoid Cotesia marginiventris. In addition, we studied the volatile-guided foraging behavior of C. marginiventris to explore whether nutrient stress affects the plant's indirect defense. Our results show that photosynthetic efficiency, leaf N, and soluble protein content were significantly reduced in N deficient plants whereas root biomass was increased. Nitrogen starved plants emitted the same range of herbivore-induced VOCs as control plants, but quantitative changes occurred in the release of the main compound and two other volatiles. Herbivore growth and the performance of parasitoids developing inside the affected hosts were attenuated when caterpillars fed on N deficient plants. The behavioral response of C. marginiventris to induced VOCs from N deficient hosts, however, remained unaffected. In summary, N stress had strong bottom-up effects over three trophic levels, but the plant's indirect defense remained intact.