The influence of below-ground herbivory and defoliation of a legume on nitrogen transfer to neighbouring plants

1. Both foliar and root herbivory can alter the exudation of carbon from plant roots, which in turn can affect nitrogen availability in the soil. However, few studies have investigated the effects of herbivory on N fluxes from roots, which can directly increase N availability in the soil and uptake by neighbouring plants. Moreover, the combined effects of foliar and root herbivory on N fluxes remains unexplored. 2. We subjected the legume white clover (Trifolium repens L.) to defoliation (through clipping) and root herbivory (by an obligate root-feeding nematode, Heterodera trifolii Goggart) to examine how these stresses individually, and simultaneously, affected the transfer of T. repens-derived N to neighbouring perennial ryegrass (Lolium perenne L.) plants using N-15 stable-isotope techniques. We also examined the effects of defoliation and root herbivory on the size of the soil microbial community and the growth response of L. perenne. 3. Neither defoliation nor root herbivory negatively affected T. repens biomass. On the contrary, defoliation increased root biomass (34%) and total shoot production by T. repens (100%). Furthermore, defoliation resulted in a fivefold increase in T. repens-derived N-15 recovered in L. perenne roots, and increased the size of the soil microbial biomass (77%). In contrast, root herbivory by H. trifolii slightly reduced N-15 transfer from T. repens to L. perenne when T. repens root N-15 concentration was included as a covariate, and root herbivory did not affect microbial biomass. Growth of L. perenne was not affected by any of the treatments. 4. Our findings demonstrate that defoliation of a common grassland legume can substantially increase the transfer of its N to neighbouring plants by directly affecting below-ground N fluxes. These finding require further examination under field conditions but, given the prevalence of N-limitation of plant productivity in terrestrial ecosystems, increased transfer of N from legumes to non-N-fixing species could alter competitive interactions, with implications for plant community structure.