While shoot herbivory mitigates, root herbivory exacerbates eutrophication’s impact on diversity in a grassland model

1AbstractEutrophication is widespread throughout grassland systems and expected to increase during the Anthropocene. Trophic interactions, like aboveground herbivory, have been shown to mitigate its effect on plant diversity. Belowground herbivory may also impact these habitats’ response to eutrophication, but the direction of its influence is much less understood, and likely to depend on factors such as the herbivores’ preference for dominant species and the symmetry of belowground competition. If preferential towards the dominant, fastest growing species, root herbivores may reduce these species’ relative fitness and support diversity during eutrophication. However, as plant competition belowground is commonly considered to be symmetric, root herbivores may be less impactful than shoot herbivores because they do not reduce any competitive asymmetry between the dominant and subordinate plants.To better understand this system, we used an established, two-layer, grassland community model to run a full-factorially designed simulation experiment, crossing the complete removal of aboveground herbivores and belowground herbivores with eutrophication. After 100 years of simulation, we analyzed communities’ diversity, competition on the individual-level, as well as their resistance and recovery. The model reproduced both observed general effects of eutrophication in grasslands and the short-term trends of specific experiments. We found that belowground herbivores exacerbate the negative influence of eutrophication on Shannon diversity within our model grasslands, while aboveground herbivores mitigate its effect. Indeed, data on individuals’ above- and belowground resource uptake reveals that root herbivory reduces resource limitation belowground. As with eutrophication, this shifts competition aboveground. Since shoot competition is asymmetric—with larger, taller individuals gathering disproportionate resources compared to their smaller, shorter counterparts—this shift promotes the exclusion of the smallest species. While increasing the root herbivores’ preferences towards dominant species lessens their negative impact, at best they are only mildly advantageous, and they do very little reduce the negative consequences of eutrophication. Because our model’s belowground competition is symmetric, we hypothesize that root herbivores may be beneficial when root competition is asymmetric. Future research into belowground herbivory should account for the nature of competition belowground to better understand the herbivores’ true influence.