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Symbiotic dinoflagellates divert energy away from mutualism during coral bleaching recovery

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Abstract

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.

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Data availability

Data and R code are available on GitHub at github.com/allenwaller/MontiporaSymbStrategy.

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Acknowledgements

We thank Teegan Innis, Crawford Drury, Josh Hancock, Ariana Huffmyer, Shayle Matsuda, Mindy Mizobe, and the staff of the Hawai’i Institute of Marine Biology for logistical support during the experiment; Christopher Carlson for image analysis assistance; Christopher Wall for indispensable isotope advice; and the staff of the UC-Davis Stable Isotope Lab for isotope analysis. Corals were collected under Special Activity Permit 2020-41. This work was supported by the NIH T32 Predoctoral Training Grant in Cell and Molecular Biology GM-07229 to L.A.-W., NSF-OCE 1923743 to K.L.B, Charles E. Kaufman Foundation New Investigator Award KA2021-114797 to K.L.B., and funding from the University of Pennsylvania to K.L.B.

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    Luella Allen-Waller & Katie L. Barott

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L.A.-W. and K.L.B. conceived and designed the study. L.A.-W. collected samples, prepared materials, collected and analyzed data, and wrote the first draft of the manuscript. K.L.B. collected and analyzed data, and edited and approved the final manuscript.

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Correspondence to Katie L. Barott.

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Allen-Waller, L., Barott, K.L. Symbiotic dinoflagellates divert energy away from mutualism during coral bleaching recovery. Symbiosis 89, 173–186 (2023). https://doi.org/10.1007/s13199-023-00901-3

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