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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 treat- ment 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 endos- ymbiosis 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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Heat stress and bleaching in corals: a bioenergetic model
Abstract The coral-dinoflagellate endosymbiosis is based on nutrient exchanges that impact holobiont energetics. Of particular concern is the breakdown or dysbiosis of this partnership that is seen in response to elevated temperatures, where loss of symbionts through coral bleaching can lead to starvation and mortality. Here we extend a dynamic bioenergetic model of coral symbioses to explore the mechanisms by which temperature impacts various processes in the symbiosis and to enable simulational analysis of thermal bleaching. Our model tests the effects of two distinct mechanisms for how increased temperature impacts the symbiosis: 1) accelerated metabolic rates due to thermodynamics and 2) damage to the photosynthetic machinery of the symbiont caused by heat stress. Model simulations show that the model can capture key biological responses to different levels of increased temperatures. Moderately increased temperatures increase metabolic rates and slightly decrease photosynthesis. The slightly decreased photosynthesis rates cause the host to receive less carbon and share more nitrogen with the symbiont. This results in temporarily increased symbiont growth and a higher symbiont/host ratio. In contrast, higher temperatures cause a breakdown of the symbiosis due to escalating feedback that involves further reduction in photosynthesis and insufficient energy supply for$$\hbox {CO}_2$$ concentration by the host. This leads to the accumulation of excess light energy and the generation of reactive oxygen species, eventually triggering symbiont expulsion and coral bleaching. Importantly, bleaching does not result from accelerated metabolic rates alone; it only occurs as a result of the photodamage mechanism due to its effect on nutrient cycling. Both higher light intensities and higher levels of DIN render corals more susceptible to heat stress. Conversely, heterotrophic feeding can increase the maximal temperature that can be tolerated by the coral. Collectively these results show that a bioenergetics model can capture many observed patterns of heat stress in corals, such as higher metabolic rates and higher symbiont/host ratios at moderately increased temperatures and symbiont expulsion at strongly increased temperatures.
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- Award ID(s):
- 2224354
- PAR ID:
- 10552934
- Publisher / Repository:
- Springer Science + Business Media
- Date Published:
- Journal Name:
- Coral Reefs
- Volume:
- 43
- Issue:
- 6
- ISSN:
- 0722-4028
- Format(s):
- Medium: X Size: p. 1627-1645
- Size(s):
- p. 1627-1645
- Sponsoring Org:
- National Science Foundation
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