Microalgal blooms in the skeletons of bleached corals during the 2020 bleaching event on Heron Island, Australia
A. J. Fordyce![https://orcid.org/0000-0002-8577-8174](/media/client/orcid_16x16.png)
![https://orcid.org/0000-0001-6476-9263](/media/client/orcid_16x16.png)
A University of Newcastle, School of Environmental and Life Sciences, Callaghan, NSW 2309, Australia.
B School of Biological, Earth and Environmental Sciences, Level 5, UNSW Sydney, Kensington, NSW 1466, Australia.
C Corresponding author. Email: alexander.fordyce@uon.edu.au
Marine and Freshwater Research 72(11) 1689-1694 https://doi.org/10.1071/MF21050
Submitted: 11 February 2021 Accepted: 12 June 2021 Published: 12 July 2021
Journal Compilation © CSIRO 2021 Open Access CC BY-NC-ND
Abstract
Climate change is increasing the frequency of marine heatwaves around the world, causing widespread degradation of coral reefs. Endolithic microalgae inhabiting the coral skeleton have been highlighted as potentially important mediators of the consequences of heatwaves on coral reefs. These microalgae often bloom during heat stress due to greater light availability, theoretically delaying coral starvation by providing photoassimilates. However, these microalgae also dissolve coral skeletons at an accelerated rate during marine heatwaves, affecting the structural complexity of the reef. Despite their ecological role, no studies have examined endolithic algal blooms during a natural bleaching event. We quantified blooms of endolithic microalgae in the skeletons of lagoon corals bleaching on Heron Island in the austral summer of 2020. At the peak of heat stress, 20–30% of bleached corals across 9 genera at 3 sites had blooms. They were predominantly seen in branching Acropora spp. (37.8, 65.7 and 66.7% at three sites), which are primary reef builders at Heron Island. At the end of the bleaching event, the overall prevalence varied between 5 and 42%, and nearly all blooms were observed in acroporids. The relative high frequency of these blooms highlights the ongoing need to understand the role of these microbes during coral bleaching events.
References
Abràmoff, M. D., Magalhães, P. J., and Ram, S. J. (2004). Image processing with Image. J. Biophotonics International 11, 36–42.Ainsworth, T. D., Leggat, W., Silliman, B. R., Lantz, C. A., Bergman, J. L., Fordyce, A. J., Page, C. E., Renzi, J. J., Morton, J., Eakin, C. M., and Heron, S. F. (in press). Rebuilding relationships on coral reefs. Coral bleaching knowledge-sharing to aid adaptation planning for coral reef users. BioEssays , .
Bahr, K. D., Jokiel, P. L., and Rodgers, K. S. (2016). Influence of solar irradiance on underwater temperature recorded by temperature loggers on coral reefs. Limnology and Oceanography, Methods 14, 338–342.
| Influence of solar irradiance on underwater temperature recorded by temperature loggers on coral reefs.Crossref | GoogleScholarGoogle Scholar |
Bryson, M., Ferrari, R., Figueira, W., Pizarro, O., Madin, J., Williams, S., and Byrne, M. (2017). Characterization of measurement errors using structure‐from‐motion and photogrammetry to measure marine habitat structural complexity. Ecology and Evolution 7, 5669–5681.
| Characterization of measurement errors using structure‐from‐motion and photogrammetry to measure marine habitat structural complexity.Crossref | GoogleScholarGoogle Scholar | 28808546PubMed |
Carilli, J. E., Godfrey, J., Norris, R. D., Sandin, S. A., and Smith, J. E. (2010). Periodic endolithic algal blooms in Montastraea faveolata corals may represent periods of low-level stress. Bulletin of Marine Science 86, 709–718.
del Campo, J., Pombert, J.-F., Šlapeta, J., Larkum, A., and Keeling, P. J. (2017). The ‘other’ coral symbiont: ostreobium diversity and distribution. The ISME Journal 11, 296–299.
| The ‘other’ coral symbiont: ostreobium diversity and distribution.Crossref | GoogleScholarGoogle Scholar | 27420029PubMed |
Diaz-Pulido, G., and McCook, L. J. (2002). The fate of bleached corals: patterns and dynamics of algal recruitment. Marine Ecology Progress Series 232, 115–128.
| The fate of bleached corals: patterns and dynamics of algal recruitment.Crossref | GoogleScholarGoogle Scholar |
Fine, M., and Loya, Y. (2002). Endolithic algae: an alternative source of photoassimilates during coral bleaching. Proceedings Biological Sciences 269, 1205–1210.
| Endolithic algae: an alternative source of photoassimilates during coral bleaching.Crossref | GoogleScholarGoogle Scholar | 12065035PubMed |
Fine, M., Meroz-Fine, E., and Hoegh-Guldberg, O. (2005). Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef. The Journal of Experimental Biology 208, 75–81.
| Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar | 15601879PubMed |
Fine, M., Roff, G., Ainsworth, T. D., and Hoegh-Guldberg, O. (2006). Phototrophic microendoliths bloom during coral ‘white syndrome’. Coral Reefs 25, 577–581.
| Phototrophic microendoliths bloom during coral ‘white syndrome’.Crossref | GoogleScholarGoogle Scholar |
Fordyce, A. J., Ainsworth, T. D., Heron, S. F., and Leggat, W. (2019). Marine heatwave hotspots in coral reef environments: physical drivers, ecophysiological outcomes and impact upon structural complexity. Frontiers in Marine Science 6, 498.
| Marine heatwave hotspots in coral reef environments: physical drivers, ecophysiological outcomes and impact upon structural complexity.Crossref | GoogleScholarGoogle Scholar |
Fordyce, A., Ainsworth, T., and Leggat, W. (2021). Light capture, skeletal morphology, and the biomass of corals’ boring endoliths. MSphere 6, e00060-21.
| Light capture, skeletal morphology, and the biomass of corals’ boring endoliths.Crossref | GoogleScholarGoogle Scholar | 33627505PubMed |
Graham, N. A. J., and Nash, K. L. (2013). The importance of structural complexity in coral reef ecosystems. Coral Reefs 32, 315–326.
| The importance of structural complexity in coral reef ecosystems.Crossref | GoogleScholarGoogle Scholar |
Great Barrier Reef Marine Park Authority (2020). Statement: coral bleaching on the Great Barrier Reef. (GBRMPA.) Available at https://www.gbrmpa.gov.au/news-room/latest-news/latest-news/coral-bleaching/2020/statement-coral-bleaching-on-the-great-barrier-reef
Gutiérrez-Isaza, N., Espinoza-Avalos, J., León-Tejera, H., and González-Solís, D. (2015). Endolithic community composition of Orbicella faveolata (Scleractinia) underneath the interface between coral tissue and turf algae. Coral Reefs 34, 625–630.
| Endolithic community composition of Orbicella faveolata (Scleractinia) underneath the interface between coral tissue and turf algae.Crossref | GoogleScholarGoogle Scholar |
Hobday, A. J., Alexander, L. V., Perkins, S. E., Smale, D. A., Straub, S. C., Oliver, E. C. J., Benthuysen, J. A., Burrows, M. T., Donat, M. G., Feng, M., Holbrook, N. J., Moore, P. J., Scannell, H. A., Sen Gupta, A., and Wernberg, T. (2016). A hierarchical approach to defining marine heatwaves. Progress in Oceanography 141, 227–238.
| A hierarchical approach to defining marine heatwaves.Crossref | GoogleScholarGoogle Scholar |
Hughes, T. P., Kerry, J. T., Baird, A. H., Connolly, S. R., Dietzel, A., Eakin, C. M., Heron, S. F., Hoey, A. S., Hoogenboom, M. O., and Liu, G. (2018). Global warming transforms coral reef assemblages. Nature 556, 492–496.
| Global warming transforms coral reef assemblages.Crossref | GoogleScholarGoogle Scholar | 29670282PubMed |
Joyce, K. E., Phinn, S. R., and Roelfsema, C. M. (2013). Live coral cover index testing and application with hyperspectral airborne image data. Remote Sensing 5, 6116–6137.
| Live coral cover index testing and application with hyperspectral airborne image data.Crossref | GoogleScholarGoogle Scholar |
Le Campion-Alsumard, T., Golubic, S., and Priess, K. (1995). Fungi in corals: symbiosis or disease? Interaction between polyps and fungi causes pearl-like skeleton biomineralization. Marine Ecology Progress Series 117, 137–147.
| Fungi in corals: symbiosis or disease? Interaction between polyps and fungi causes pearl-like skeleton biomineralization.Crossref | GoogleScholarGoogle Scholar |
Leggat, W. P., Camp, E. F., Suggett, D. J., Heron, S. F., Fordyce, A. J., Gardner, S., Deakin, L., Turner, M., Beeching, L. J., Kuzhiumparambil, U., Eakin, C. M., and Ainsworth, T. D. (2019). Rapid coral decay is associated with marine heatwave mortality events on reefs. Current Biology 29, 2723–2730.e4.
| Rapid coral decay is associated with marine heatwave mortality events on reefs.Crossref | GoogleScholarGoogle Scholar | 31402301PubMed |
Liu, G., Heron, F. S., Eakin, M. C., Muller-Karger, E. F., Vega-Rodriguez, M., Guild, S. L., De La Cour, L. J., Geiger, F. E., Skirving, J. W., Burgess, F. T., Strong, E. A., Harris, A., Maturi, E., Ignatov, A., Sapper, J., Li, J., and Lynds, S. (2014). Reef-scale thermal stress monitoring of coral ecosystems: new 5-km global products from NOAA Coral Reef Watch. Remote Sensing 6, 11579–11606.
| Reef-scale thermal stress monitoring of coral ecosystems: new 5-km global products from NOAA Coral Reef Watch.Crossref | GoogleScholarGoogle Scholar |
MacKellar, M. C., and McGowan, H. A. (2010). Air-sea energy exchanges measured by eddy covariance during a localised coral bleaching event, Heron Reef, Great Barrier Reef, Australia. Geophysical Research Letters 37, L24703.
| Air-sea energy exchanges measured by eddy covariance during a localised coral bleaching event, Heron Reef, Great Barrier Reef, Australia.Crossref | GoogleScholarGoogle Scholar |
Pernice, M., Raina, J.-B., Rädecker, N., Cárdenas, A., Pogoreutz, C., and Voolstra, C. R. (2020). Down to the bone: the role of overlooked endolithic microbiomes in reef coral health. The ISME Journal 14, 325–334.
| Down to the bone: the role of overlooked endolithic microbiomes in reef coral health.Crossref | GoogleScholarGoogle Scholar | 31690886PubMed |
Perry, C. T., Murphy, G. N., Kench, P. S., Edinger, E. N., Smithers, S. G., Steneck, R. S., and Mumby, P. J. (2014). Changing dynamics of Caribbean reef carbonate budgets: emergence of reef bioeroders as critical controls on present and future reef growth potential. Proceedings of the Royal Society of London. Series B, Biological Sciences 281, 2014–2018.
Ricci, F., Marcelino, V. R., Blackall, L. L., Kühl, M., Medina, M., and Verbruggen, H. (2019). Beneath the surface: community assembly and functions of the coral skeleton microbiome. Microbiome 7, 159.
| Beneath the surface: community assembly and functions of the coral skeleton microbiome.Crossref | GoogleScholarGoogle Scholar | 31831078PubMed |
Risk, M. J., and Muller, H. R. (1983). Porewater in coral heads: evidence for nutrient regeneration 1. Limnology and Oceanography 28, 1004–1008.
| Porewater in coral heads: evidence for nutrient regeneration 1.Crossref | GoogleScholarGoogle Scholar |
Ruiz-Jones, L. J., and Palumbi, S. R. (2017). Tidal heat pulses on a reef trigger a fine-tuned transcriptional response in corals to maintain homeostasis. Science Advances 3, e1601298.
| Tidal heat pulses on a reef trigger a fine-tuned transcriptional response in corals to maintain homeostasis.Crossref | GoogleScholarGoogle Scholar | 28345029PubMed |
Sangsawang, L., Casareto, B. E., Ohba, H., Vu, H. M., Meekaew, A., Suzuki, T., Yeemin, T., and Suzuki, Y. (2017). 13C and 15N assimilation and organic matter translocation by the endolithic community in the massive coral Porites lutea. Royal Society Open Science 4, 171201.
| 13C and 15N assimilation and organic matter translocation by the endolithic community in the massive coral Porites lutea.Crossref | GoogleScholarGoogle Scholar | 29308251PubMed |
Schlichter, D., Zscharnack, B., and Krisch, H. (1995). Transfer of photoassimilates from endolithic algae to coral tissue. Naturwissenschaften 82, 561–564.
| Transfer of photoassimilates from endolithic algae to coral tissue.Crossref | GoogleScholarGoogle Scholar |
Swain, T. D., Vega-Perkins, J. B., Oestreich, W. K., Triebold, C., DuBois, E., Henss, J., Baird, A., Siple, M., Backman, V., and Marcelino, L. (2016). Coral bleaching response index: a new tool to standardize and compare susceptibility to thermal bleaching. Global Change Biology 22, 2475–2488.
| Coral bleaching response index: a new tool to standardize and compare susceptibility to thermal bleaching.Crossref | GoogleScholarGoogle Scholar | 27074334PubMed |
Traylor-Knowles, N., Rose, N. H., Sheets, E. A., and Palumbi, S. R. (2017). Early transcriptional responses during heat stress in the coral Acropora hyacinthus. The Biological Bulletin 232, 91–100.
| Early transcriptional responses during heat stress in the coral Acropora hyacinthus.Crossref | GoogleScholarGoogle Scholar | 28654330PubMed |
Voolstra, C. R., and Ziegler, M. (2020). Adapting with microbial help: microbiome flexibility facilitates rapid responses to environmental change. BioEssays 42, 2000004.
| Adapting with microbial help: microbiome flexibility facilitates rapid responses to environmental change.Crossref | GoogleScholarGoogle Scholar | 32548850PubMed |
Williams, A. D., Brown, B. E., Putchim, L., and Sweet, M. J. (2015). Age-related shifts in bacterial diversity in a reef coral. PLoS One 10, e0144902.
| Age-related shifts in bacterial diversity in a reef coral.Crossref | GoogleScholarGoogle Scholar | 26700869PubMed |
Ziegler, M., Grupstra, C. G., Barreto, M. M., Eaton, M., BaOmar, J., Zubier, K., Al-Sofyani, A., Turki, A. J., Ormond, R., and Voolstra, C. R. (2019). Coral bacterial community structure responds to environmental change in a host-specific manner. Nature Communications 10, 3092.
| Coral bacterial community structure responds to environmental change in a host-specific manner.Crossref | GoogleScholarGoogle Scholar | 31300639PubMed |