Coastal ecosystems are generally controlled by the combination of bottom-up (resourcedriven) and top-down (consumer-driven) trophic, and non-trophic interactions. Anthropogenic disruption of these interactions, e.g., through eutrophication or overfishing, leads to loss of the foundation species composing these ecosystems. Within degraded ecosystems, new interactions may become dominant, hampering restoration of foundation species.

We demonstrate this concept in saltwater Lake Grevelingen, where seagrass restoration was seriously hampered by a newly discovered non-trophic interaction between the seagrass Zostera marina and the ragworm Platynereis dumerilii. Platynereis constructs dwelling tubes between seagrass leaves by gluing and entangling them, leading to loss of biomass and increased epiphyte cover. To test the roles of epiphyte grazing (top-down) and eutrophication (bottom-up) on this newfound interaction, we executed a field experiment introducing the snail Littorina littorea under natural nutrient concentrations and Platynereis densities, and performed a full factorial mesocosm experiment applying Littorina, Platynereis and nutrient treatments.

Our field results show that survival of reintroduced Zostera in Lake Grevelingen is seriously hampered by Platynereis, which can be suppressed by grazer addition.

In our mesocosm experiment we demonstrate that top-down control by Littorina protected seagrass through two pathways: (1) mitigating bottom-up regulated epiphyte growth by trophic top-down forcing and (2) hampering the non-trophic interaction between Zostera and Platynereis by grazing epiphytes and dwelling tubes.

Synthesis and applications. With coastal ecosystems globally under pressure, our study emphasises the importance of understanding ecosystem-specific trophic and non-trophic key interactions when considering restoration. We show how negative interspecific interactions can become dominant in the absence of key facilitating interactions. Next, we show that negative interactions (leaf gluing), inhibiting foundation species restoration, can be overruled by the inclusion of positive interspecific interactions (epiphyte grazing by mesograzers). Finally, we provide a three-step co-introduction approach for restoration management.