A healthy trophic structure underlies the resistance of pristine seagrass beds to nutrient enrichment

Whether pristine ecosystems with intact trophic structures are more resilient to anthropogenic pressures than ecosystems facing human exploitation is a pressing question to ecological theory and management. For coastal vegetated ecosystems such as kelp forests and seagrass meadows, a number of studies recently highlighted that under eutrophic conditions, trophic cascades are particularly important in buffering or reducing negative effects of nutrient enrichment. Yet, it currently remains unclear how nutrient enrichment and trophic downgrading interact in oligotrophic coastal ecosystems with an intact trophic structure. Here, we factorially manipulated nutrient loading and the interactions within a tri-trophic food chain within a pristine, oligotrophic seagrass ecosystem to investigate how trophic downgrading affects its ability to buffer against eutrophication. Results revealed that nutrient addition stimulates seagrass production, while reducing the growth of benthic microalgae, presumably because the thicker seagrass canopy reduced light availability. Trophic downgrading by excluding predators, however, almost completely negated these nutrient effects, as the release of herbivores from predation strongly enhanced grazing pressure on seagrass. Exclusion of grazers in turn restored seagrass biomass by allowing the nutrient addition treatment to regain its effect, confirming that a tri-trophic cascade mediated how enhanced nutrient loading affected our system. Our results highlight that a healthy trophic structure is vital for the ability of pristine coastal ecosystems to buffer eutrophication, as trophic downgrading may degrade their ability to absorb enhanced nutrient loading. Hence, our findings emphasize the potential for multiple anthropogenic impacts to interact synergistically in degrading natural ecosystems.