Symbiotic dinoflagellates divert energy away from mutualism during coral bleaching recovery

The future of coral reefs in a warming world depends on corals’ ability to recover from bleaching, the loss of their symbiotic dinoflagellate algae (Symbiodiniaceae) during marine heatwaves. Heat-tolerant symbiont species can remain in symbiosis during heat stress, but often provide less photosynthate to the host than heat-sensitive species under ambient conditions. Understanding how heat stress changes the dynamics of this tradeoff between stress tolerance and mutualism contribution is crucial for predicting coral success under climate change. To test how symbiont resource allocation affects coral recovery from heat stress, we exposed the coral Montipora capitata hosting either heat-sensitive Cladocopium C31 (C) or heat-tolerant Durusdinium glynnii (D) to heat stress. D regained symbiont density and photochemical efficiency faster after heat treatment than C, but symbiont recovery did not restore coral biomass or calcification rates to pre-bleaching levels in the initial recovery period. D populations also contributed less photosynthate to the host relative to C, even during heat stress. Further, higher-density symbiont populations of both species retained more photosynthate than lower-density populations, and corals receiving less photosynthate exhibited reduced calcification rates and lower intracellular pH. This is the first evidence that symbiont density and carbon translocation are negatively related, and the first to establish a link between Symbiodiniaceae carbon translocation and coral cellular homeostasis. Together, these results suggest the energy demand of symbiont regrowth after bleaching reduces their mutualism contribution and can thus delay host recovery. Reestablishing a beneficial endosymbiosis imposes additional costs as holobionts overcome stress, and may explain latent mortality among coral populations after alleviation of heat stress in the field.