Quantifying the impact of above- and belowground higher trophic levels on plant and herbivore performance by modeling

Growing empirical evidence suggests that aboveground and belowground multitrophic communities interact. However, investigations that comprehensively explore the impacts of above- and belowground third and higher trophic level organisms on plant and herbivore performance are thus far lacking. We tested the hypotheses that above- and belowground higher trophic level organisms as well as decomposers affect plant and herbivore performance and that these effects cross the soil-surface boundary. We used a well-validated simulation model that is individual-based for aboveground trophic levels such as shoot herbivores, parasitoids, and hyperparasitoids while considering belowground herbivores and their antagonists at the population level. We simulated greenhouse experiments by removing trophic levels and decomposers from the simulations in a factorial design. Decomposers and above- and belowground third trophic levels affected plant and herbivore mortality, root biomass, and to a lesser extent shoot biomass. We also tested the effect of gradual modifications of the interactions between different trophic level organisms with a sensitivity analysis. Shoot and root biomass were highly sensitive to the impact of the fourth trophic level. We found effects that cross the soil surface, such as aboveground herbivores and parasitoids affecting root biomass and belowground herbivores influencing aboveground herbivore mortality. We conclude that higher trophic level organisms and decomposers can strongly influence plant and herbivore performance. We propose that our modelling framework can be used in future applications to quantitatively explore the possible outcomes of complex above- and belowground multitrophic interactions under a range of environmental conditions and species compositions.