Water-mediated productivity dynamics in shifting coral reef communities

Abstract

Mass mortality of reef-building stony corals has driven widespread community shifts towards reefs dominated by soft corals and macroalgae. Although physical competition for space between these organisms plays an important role, non-contact water-mediated interactions have been proposed to modulate organismal performance and community functioning, yet their independent effects remain poorly resolved. Here, we experimentally tested the hypothesis that water-mediated interactions generate non-additive effects on community productivity, altering ecosystem functioning during phase shifts. Using two controlled incubation experiments with representative stony corals, soft corals, and macroalgae, we compared monoculture baseline productivity with mixed assemblages across a gradient of biomass ratios mimicking phase shift scenarios. We found that reductions in stony coral biomass led to community-level declines in photosynthesis and calcification that exceeded expectations based on monocultures, indicating emergent negative effects of community restructuring. However, these effects were strongly species-dependent, with some assemblages showing only minor deviations from expectations, whereas others exhibited pronounced productivity losses. At the species level, both stony corals reduced photosynthetic efficiency in mixed assemblages, while soft corals maintained efficiency across treatments. Macroalgal responses diverged, with one species exhibiting reduced and another increased photosynthetic efficiency in mixed communities. These species-specific physiological responses scaled up to explain community-level deviations from expected productivity, suggesting that gains in productivity by certain taxa can partially offset, but not fully compensate for, losses in coral-driven functions such as calcification. Together, our findings indicate that sublethal, water-mediated interactions can reorganize holobiont functioning and lead to changes in ecosystem productivity, independent of direct physical competition. By altering community-wide energy acquisition and carbonate production, such interactions may reinforce feedback loops that accelerate ecosystem phase shifts. We argue that incorporating water-mediated interaction effects into ecological theory and ecosystem models is essential for predicting the stability and recovery potential of coral reefs and other transitioning ecosystems under climate change.