Community metabolism generates chemical legacies that alter coral physiology

Abstract

Coral reefs are among the world's most diverse ecosystems and contribute substantially to ocean productivity and the carbon budget. Disturbances are shifting reefs to altered community states, yet how these new communities indirectly alter organismal physiology by modifying the local biogeochemical environment remains largely unknown. We investigated this biogeochemical feedback in a 25‐d mesocosm experiment in Mo'orea, French Polynesia. We exposed the common coral Porites rus to the biogeochemical environments generated by three distinct communities representative of recent benthic states in this system: coral‐, macroalgae‐, and crustose coralline algae‐enriched relative to a seawater‐only control. While net community production was similar among communities, net community calcification was lowest in the macroalgae‐enriched state. Across treatments, community metabolism drove changes in the organic and inorganic carbon pool, with net community production increasing both pH and dissolved organic carbon. Using structural equation modeling, we tested how these community‐generated chemical legacies propagated through coral physiology. Elevated pH increased chlorophyll a content, which increased endosymbiont density, tissue biomass, gross photosynthesis, and respiration through a series of indirect pathways. Dissolved organic carbon had no detectable effect on downstream corals at 25 d. These results reveal a mechanistic pathway linking disturbance‐driven shifts in benthic communities to coral performance. Altered community metabolism modifies local carbon chemistry, which reshapes symbiont physiology and ultimately influences host metabolic function. By identifying the pathways through which community states engineer their chemical environment, this study provides a framework for predicting coral performance and ecosystem trajectories as reefs transition away from coral‐enriched states.