Overfishing of top predators eroded the resilience of the Black Sea system regardless of the climate and anthropogenic conditions

It is well known that human activities, such as harvesting, have had major direct effects on marine ecosystems. However, it is far less acknowledged that human activities in the surroundings might have important effects on marine systems. There is growing evidence suggesting that major reorganization (i.e., a regime shift) is a common feature in the temporal evolution of a marine system. Here we show, and quantify, the interaction of human activities (nutrient upload) with a favourable climate (run-off) and its contribution to the eutrophication of the Black Sea in the 1980s. Based on virtual analysis of the bottom-up (eutrophication) vs. top-down (trophic cascades) effects, we found that an earlier onset of eutrophication could have counteracted the restructuring of the trophic regulation at the base of the food web that resulted from the depletion of top predators in the 1970s. These enhanced bottom-up effects would, however, not propagate upwards in the food web beyond the zooplankton level. Our simulations identified the removal of apex predators as a key element in terms of loss of resilience that inevitably leads to a reorganization. Once the food web has been truncated, the type and magnitude of interventions on the group replacing the apex predator as the new upper trophic level have no effect in preventing the trophic cascade. By characterizing the tipping point at which increased bottom-up forcing exactly counteracts the top-down cascading effects, our results emphasize the importance of a comprehensive analysis that take into account all structuring forces at play (including those beyond the marine system) at a given time.EUR-OCEANS Integration Project 2007; Marie Curie Intra-European fellowship [FP6-2005-Mobility-5]; Marie Curie European Reintegration Grant [FP7-People- 2009-RG]; EU WETLANET, KNOWSEAS, and MEECE, UK NERC QUEST; US National Science Foundation (DMS-0935617