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  • Review Article
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Extending the natural adaptive capacity of coral holobionts

Nature Reviews Earth & Environment volume 2, pages 747–762 (2021)Cite this article

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Abstract

Anthropogenic climate change and environmental degradation destroy coral reefs, the ecosystem services they provide, and the livelihoods of close to a billion people who depend on these services. Restoration approaches to increase the resilience of corals are therefore necessary to counter environmental pressures relevant to climate change projections. In this Review, we examine the natural processes that can increase the adaptive capacity of coral holobionts, with the aim of preserving ecosystem functioning under future ocean conditions. Current approaches that centre around restoring reef cover can be integrated with emerging approaches to enhance coral stress resilience and, thereby, allow reefs to regrow under a new set of environmental conditions. Emerging approaches such as standardized acute thermal stress assays, selective sexual propagation, coral probiotics, and environmental hardening could be feasible and scalable in the real world. However, they must follow decision-making criteria that consider the different reef, environmental, and ecological conditions. The implementation of adaptive interventions tailored around nature-based solutions will require standardized frameworks, appropriate ecological risk–benefit assessments, and analytical routines for consistent and effective utilization and global coordination.

Key points

  • Coral reefs are degrading globally from anthropogenic climate change and local environmental impacts; deteriorated reefs are facing severe and widespread loss without active intervention.

  • Ongoing efforts aim to extend the natural adaptive capacity of reef-forming coral holobionts through incorporation of novel tools, methods, and environments to manipulate coral adaptive responses to survive under more extreme or variable conditions.

  • Emerging nature-based adaptive approaches spur novel intervention strategies that hold the promise to be feasible and scalable in the real world but must be tailored to address the diverse reef, environmental, and ecological conditions.

  • Implementing an adaptive intervention framework focused on naturally evolved solutions will require standardized methodology, appropriate ecological risk–benefit assessments, and analytical routines for consistent and effective utilization and global coordination.

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Fig. 1: The coral holobiont (metaorganism).
Fig. 2: Adaptive processes in the coral holobiont and their utilization in adaptive interventions.
Fig. 3: A scaled adaptive intervention framework.
Fig. 4: Research road map for extending the adaptive capacity of the coral holobiont.

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Acknowledgements

C.R.V. acknowledges funding from the German Research Foundation (DFG) (grants 433042944 and 458901010). R.S.P. acknowledges funding from King Abdullah University of Science and Technology (grant FCC/1/1973-51-01). J.E.P. acknowledges funding from the University of South Florida Research & Innovation Internal Awards Program (grant 0142687). K.M.Q. acknowledges funding from the Australian Institute of Marine Science (AIMS). E.M.M. was supported by the Mote Eminent Scholarship and the National Science Foundation (NSF) (OCE-1452538). M.A. acknowledges funding from King Abdullah University of Science and Technology (grant FCC/1/1973-36-01).

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Authors and Affiliations

  1. Department of Biology, University of Konstanz, Konstanz, Germany

    Christian R. Voolstra

  2. Climate Change Cluster, Faculty of Science, University of Technology Sydney, Ultimo, New South Wales, Australia

    David J. Suggett

  3. Red Sea Research Center (RSRC), Division of Biological and Environmental Science and Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia

    Raquel S. Peixoto & Manuel Aranda

  4. Institute of Microbiology, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil

    Raquel S. Peixoto

  5. Department of Integrative Biology, University of South Florida, Tampa, FL, USA

    John E. Parkinson

  6. Australian Institute of Marine Science, Townsville, Queensland, Australia

    Kate M. Quigley & David G. Bourne

  7. Department of Biology, University of Miami, Coral Gables, FL, USA

    Cynthia B. Silveira

  8. Aquatic Research Facility, Environmental Sustainability Research Centre, University of Derby, Derby, UK

    Michael Sweet

  9. Mote Marine Laboratory, Sarasota, FL, USA

    Erinn M. Muller

  10. Department of Biological Sciences, Old Dominion University, Norfolk, VA, USA

    Daniel J. Barshis

  11. College of Science and Engineering, James Cook University, Townsville, Queensland, Australia

    David G. Bourne

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  1. Christian R. Voolstra
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  4. John E. Parkinson
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Contributions

Researching data for article: C.R.V., R.P., J.E.P., K.M.Q., C.B.S., M.S., M.A.; substantial contribution to discussion of content: C.R.V., D.J.S., R.P., J.E.P., K.M.Q., C.B.S., D.G.B., M.A.; writing: C.R.V., D.J.S., R.P., J.E.P., K.M.Q., C.B.S., D.G.B., M.A.; review/editing manuscript before submission: C.R.V., D.J.S., R.P., J.E.P., K.M.Q., C.B.S., M.S., E.M.M., D.J.B., D.G.B., M.A.

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Correspondence to Christian R. Voolstra.

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Nature Reviews Earth & Environment thanks D. Huang, who co-reviewed with E. Bollati; J. Wiedenmann; S.-L. Tang; and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Glossary

Coral bleaching

Discolouration of coral tissue due to the loss of microalgal symbionts triggered by climate change-induced ocean warming and thermal stress anomalies.

Assisted evolution

Human interventions aimed at speeding up natural evolutionary processes to increase the rate of adaptation of threatened species.

Adaptive capacity

The ability of coral holobionts to respond and adjust to environmental stress.

Acclimation

The physiological process of becoming accustomed to a new condition.

Environmental adaptation

The process of (meta-)organismal change used more broadly to denote adjustment to prevailing environmental conditions, for example in the context of host microbiome changes

Evolutionary adaptation

The process of genetic change through which populations become better attuned to their environment over generations.

Restoration

The action of returning something to a former condition, for instance through reinstatement of the original functional or genetic diversity.

Environmental hardening

The preconditioning of coral colonies to elevated temperatures as a means to increase tolerance to future heat stress events (can also apply to other stressors).

Microhabitats

A small area that differs from the surrounding habitat, with unique conditions that could select for unique genotypes that might not be found in the remainder of the area.

Beneficial Microorganisms for Corals

(BMCs). Umbrella term to define (microbial) symbionts that promote coral health and can be used as probiotics.

Coral probiotics

Live microorganisms to benefit coral host health.

Coral prebiotics

Molecules that modulate bacterial (microbial) association to benefit coral host health.

Lysis

A common outcome of viral infections, whereby cells are actively induced by viruses to release newly assembled viruses that can then infect other cells.

Genetically modified organisms

(GMOs). Organisms whose genomes are engineered to produce specific traits of interest.

Environmental rehabilitation

The action of restoring to an improved condition to allow species and ecosystems to thrive under altered environmental conditions.

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Voolstra, C.R., Suggett, D.J., Peixoto, R.S. et al. Extending the natural adaptive capacity of coral holobionts. Nat Rev Earth Environ 2, 747–762 (2021). https://doi.org/10.1038/s43017-021-00214-3

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