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Coral host physiology and symbiont dynamics associated with differential recovery from mass bleaching in an extreme, macro-tidal reef environment in northwest Australia

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Abstract

As marine heatwaves increasingly threaten coral reefs worldwide, some extreme reef environments naturally expose corals to high-temperature fluctuations and can therefore provide important insights into the mechanisms underlying coral heat tolerance. Coral reefs in the Kimberley region in northwest Australia experience the world’s largest tropical tides and are therefore exposed to highly fluctuating temperatures in the intertidal. In contrast, the subtidal remains mostly submerged, resulting in moderate daily temperature fluctuations. A marine heatwave in 2016 triggered wide-spread bleaching in the Kimberley. Intertidal corals bleached less and recovered faster than adjacent subtidal corals; however, the mechanisms underlying this differential bleaching and recovery response remain poorly understood. Here we assessed both host- and symbiont-based indicators of bleaching resilience in the coral Acropora aspera. We tagged visibly healthy and bleached colonies from both environments in April 2016 and measured symbiont community composition, cell density, chlorophyll a, total biomass and host tissue energy reserves (lipids, protein and carbohydrates) during bleaching in April and in November 2016. Bleaching severity was higher in the subtidal than in intertidal, and while Cladocopium dominated all corals, symbiont community compositions differed significantly between environments and between bleached and healthy subtidal corals. Interestingly, bleaching resilience seemed decoupled from energy reserves, even though high levels of energy reserves and/or sufficient consumption during bleaching are widely thought to increase resistance to and recovery from bleaching. Although all bleached/recovered corals showed a general pattern of catabolizing protein reserves, distinct environment-specific trends were observed: subtidal corals that suffered extensive mortality also catabolized energy-poor carbohydrate reserves. In contrast, intertidal corals recovered rapidly after bleaching and maintained energy reserves. Total biomass remained unchanged between bleached and healthy corals in both environments. Overall, the findings of this study demonstrate that the consumption of energy reserves during bleaching is not always a reliable indicator of bleaching resilience.

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Fig. 1
Fig. 2

reproduced from Schoepf et al. 2020) and symbiont density (e, f) ± standard error (SE) of Acropora aspera. SE is missing for bleached/recovered subtidal corals in November 2016 as sample size was one (Table S3). Asterisks indicate significant differences between healthy and bleached/recovered corals within each environment. Significant environment (envo), health and time effects are indicated when present (Table S4). Note that the health status refers to the assessment in April 2016

Fig. 3

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Data will be submitted to www.pangea.de after publication.

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Acknowledgements

We thank C. Cornwall, S. Comeau, A. Kuret, A.-M. Nisumaa-Comeau, D. Thompson, M. Le Nohaïc , X. Chen, T. DeCarlo, J. Brown, G. Firman and the staff at Cygnet Bay Pearl Farm for field and laboratory assistance, A. Meenakshisundaram for assistance with genetic data analyses and Ben Hume for assistance with running samples through SymPortal. We especially thank the Bardi Jawi people who enabled this research through their advice and consent to access their traditional lands.

Funding

This study was funded by the PADI Foundation (Research Grant #21737), the University of Western Australia (Research Collaboration Award) and the Australian Research Council Centre of Excellence for Coral Reef Studies (CE140100020).

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Authors and Affiliations

  1. Oceans Graduate School and ARC Centre of Excellence for Coral Reef Studies, The University of Western Australia, 35 Stirling Highway, Perth, WA, 6009, Australia

    E. Maria U. Jung & Verena Schoepf

  2. Indian Ocean Marine Research Centre, The UWA Oceans Institute, The University of Western Australia, 35 Stirling Highway, Perth, WA, 6009, Australia

    E. Maria U. Jung, Luke Thomas & Verena Schoepf

  3. Department of Biology and Chemistry, University of Bremen, Bibliothekstraße 1, 28359, Bremen, Germany

    E. Maria U. Jung

  4. School of Environmental and Life Sciences, The University of Newcastle, University Dr,, Callaghan, NSW, 2308, Australia

    Michael Stat

  5. Indian Ocean Marine Research Centre, Australian Institute of Marine Science, 64 Fairway, Perth, WA, 6009, Australia

    Luke Thomas

  6. Trace and Environmental DNA (TrEnD) Laboratory, School of Molecular and Life Sciences, Curtin University, Kent St, Perth, WA, 6102, Australia

    Adam Koziol

  7. Faculty of Health and Medical Sciences, Center for Evolutionary Hologenomics, GLOBE Institute, University of Copenhagen, Øster Farimagsgade 5A, building 7, 2nd floor, 1353, Copenhagen, Denmark

    Adam Koziol

  8. Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1098, XH, Amsterdam, The Netherlands

    Verena Schoepf

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  1. E. Maria U. Jung
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Contributions

VS designed the study and led the field work. MJ conducted the physiological analyses, while LT, MJ, AK and MS conducted the genetic analyses. MJ executed the data analyses and statistical analyses with input from VS, LT and MS. MJ led the writing of the paper, with all co-authors contributing to the final manuscript.

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Correspondence to E. Maria U. Jung.

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Corals were collected using exemption #2549 from the Western Australia Department of Fisheries.

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Jung, E.M.U., Stat, M., Thomas, L. et al. Coral host physiology and symbiont dynamics associated with differential recovery from mass bleaching in an extreme, macro-tidal reef environment in northwest Australia. Coral Reefs 40, 893–905 (2021). https://doi.org/10.1007/s00338-021-02094-x

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