Root herbivory controls the effects of water availability on the partitioning between above- and below-ground grass biomass

The fraction of primary productivity allocated below-ground accounts for a larger flow of carbon than above-ground productivity in most grassland ecosystems. Here, we addressed the question of how root herbivory affects below-ground allocation of a dominant shortgrass prairie grass in response to water availability. We predicted that high levels of root herbivory by nematodes, as seen under extreme drought in sub-humid grasslands, would prevent the high allocation to root biomass normally expected in response to low water availability. We exposed blue grama Bouteloua gracilis, which accounts for most of the net primary productivity in the shortgrass steppe of the central and southern Great Plains, to three levels of water availability from extreme low to intermediate and extreme high crossed with a gradient of root­herbivore per cent abundance relative to the total nematode community in soil microcosms. As hypothesized, the effect of water availability on below-ground biomass allocation was contingent on the proportion of root herbivores in the nematode community. The relationship between below-ground biomass allocation and water availability was negative in the absence of root herbivory, but tended to reverse with increasing abundance of root feeders. Increasing abundance of root-feeding nematodes prevented grasses from adjusting their allocation patterns towards root mass that would, in turn, increase water uptake under dry conditions. Therefore, below-ground trophic interactions weakened plant responses and increased the negative effects of drought on plants. Our work suggests that plant responses to changes in precipitation result from complex interactions between the direct effect of precipitation and indirect effects through changes in the below-ground trophic web. Such complex responses challenge current predictions of increasing plant biomass allocation below-ground in water-stressed grasslands, and deserve further investigation across ecosystems and in field conditions. A free Plain Language Summary can be found within the Supporting Information of this article.