Diverse symbiont bleaching responses are evident from 2-degree heating week bleaching conditions as thermal stress intensifies in coral
Sarah Gierz A B , Tracy D. Ainsworth
A C E and William Leggat A B D
+ Author Affiliations
- Author Affiliations
A Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Qld 4810, Australia.
B The College of Public Health, Medical and Veterinary Sciences, James Cook University, Townsville, Qld 4810, Australia.
C Biological, Earth and Environmental Sciences, UNSW Sydney, Sydney, NSW 2052, Australia.
D School of Environmental and Life Sciences, University of Newcastle, Newcastle, NSW 2308, Australia.
E Corresponding author. Email: tracy.ainsworth@unsw.edu.au
Marine and Freshwater Research 71(9) 1149-1160 https://doi.org/10.1071/MF19220
Submitted: 21 June 2019 Accepted: 22 October 2019 Published: 3 February 2020
Abstract
Coral bleaching is the dysfunction of the coral–algal endosymbiosis and is characterised as a loss of Symbiodiniaceae cells from host tissues or the loss of photosynthetic pigments. This breakdown of symbiosis occurs as a result of elevated temperature beyond the organism’s thermal threshold. The thermal tipping points within the symbiosis have not yet been well resolved, and the mechanisms underlying the various cellular processes of the corals bleaching response remain unknown. This study characterised the cellular responses of the symbiont Cladocopium sp. (syn. clade C3) within the host coral Acropora aspera during exposure to thermal stress. Exposure to temperatures between 2 and 3°C below the bleaching threshold, equating to 2-degree heating weeks (DHWs), results in changes to the symbiont cell morphology and cell division rates. Once corals were exposed to 4 DHWs, over 90% of the symbiont cells showed signs of degradation. Although sub-bleaching thermal stress is not sufficient to trigger bleaching alerts at an ecological scale, this stressor substantially affects the coral symbiosis. It is therefore vital that we begin to quantify how sub-bleaching thermal stress affects the fitness of Symbiodiniacea populations, their coral hosts and subsequently reefs worldwide.
References
Ainsworth, T. D., Heron, S. F., Ortiz, J. C., Mumby, P. J., Grech, A., Ogawa, D., Eakin, C. M., and Leggat, W. (2016). Climate change disables coral bleaching protection on the Great Barrier Reef. Science 352, 338–342.| Climate change disables coral bleaching protection on the Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar | 27081069PubMed |
Baird, A. H., Bhagooli, R., Ralph, P. J., and Takahashi, S. (2009). Coral bleaching: the role of the host. Trends in Ecology & Evolution 24, 16–20.
| Coral bleaching: the role of the host.Crossref | GoogleScholarGoogle Scholar |
Bhagooli, R., and Hidaka, M. (2004). Release of zooxanthellae with intact photosynthetic activity by the coral Galaxea fascicularis in response to high temperature stress. Marine Biology 145, 329–337.
| Release of zooxanthellae with intact photosynthetic activity by the coral Galaxea fascicularis in response to high temperature stress.Crossref | GoogleScholarGoogle Scholar |
Brown, B. E., Le Tissier, M. D. A., and Bythell, J. C. (1995a). Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Marine Biology 122, 655–663.
| Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event.Crossref | GoogleScholarGoogle Scholar |
Brown, B. E., Le Tissier, M. D. A., and Bythell, J. C. (1995b). Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Marine Biology 122, 655–663.
| Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event.Crossref | GoogleScholarGoogle Scholar |
Coles, S. L., and Jokiel, P. L. (1978). Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Marine Biology 49, 187–195.
| Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa.Crossref | GoogleScholarGoogle Scholar |
Coles, S. L., Jokiel, P. L., and Lewis, C. (1976). Thermal tolerance in tropical versus subtropical Pacific reef corals. Pacific Science 30, 159–166.
Davies, P. S. (1984). The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi. Coral Reefs 2, 181–186.
Davy, S. K., Allemand, D., and Weis, V. M. (2012). Cell biology of cnidarian–dinoflagellate symbiosis. Microbiology and Molecular Biology Reviews 76, 229–261.
| Cell biology of cnidarian–dinoflagellate symbiosis.Crossref | GoogleScholarGoogle Scholar | 22688813PubMed |
Dimond, J. L., Pineda, R. R., Ramos-Ascherl, Z., and Bingham, B. L. (2013). Relationships between host and symbiont cell cycles in sea anemones and their symbiotic dinoflagellates. The Biological Bulletin 225, 102–112.
| Relationships between host and symbiont cell cycles in sea anemones and their symbiotic dinoflagellates.Crossref | GoogleScholarGoogle Scholar | 24243963PubMed |
Dove, S. (2004). Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Marine Ecology Progress Series 272, 99–116.
| Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching.Crossref | GoogleScholarGoogle Scholar |
Downs, C. A., Fauth, J. E., Halas, J. C., Dustan, P., Bemiss, J., and Woodley, C. M. (2002). Oxidative stress and seasonal coral bleaching. Free Radical Biology & Medicine 33, 533–543.
| Oxidative stress and seasonal coral bleaching.Crossref | GoogleScholarGoogle Scholar |
Downs, C. A., McDougall, K. E., Woodley, C. M., Fauth, J. E., Richmond, R. H., Kushmaro, A., Gibb, S. W., Loya, Y., Ostrander, G. K., and Kramarsky-Winter, E. (2013). Heat-stress and light-stress induce different cellular pathologies in the symbiotic dinoflagellate during coral bleaching. PLoS One 8, e77173.
| Heat-stress and light-stress induce different cellular pathologies in the symbiotic dinoflagellate during coral bleaching.Crossref | GoogleScholarGoogle Scholar | 24324575PubMed |
Fitt, W. K., Gates, R. D., Hoegh-Guldberg, O., Bythell, J. C., Jatkar, A., Grottoli, A. G., Gomez, M., Fisher, P., Lajuenesse, T. C., Pantos, O., Iglesias-Prieto, R., Franklin, D. J., Rodrigues, L. J., Torregiani, J. M., van Woesik, R., and Lesser, M. P. (2009). Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. Journal of Experimental Marine Biology and Ecology 373, 102–110.
| Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching.Crossref | GoogleScholarGoogle Scholar |
Franklin, D. J., Hoegh-Guldberg, O., Jones, R. J., and Berges, J. A. (2004). Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Marine Ecology Progress Series 272, 117–130.
| Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching.Crossref | GoogleScholarGoogle Scholar |
Fujise, L., Yamashita, H., Suzuki, G., Sasaki, K., Liao, L. M., and Koike, K. (2014). Moderate thermal stress causes active and immediate expulsion of photosynthetically damaged zooxanthellae (Symbiodinium) from corals. PLoS One 9, e114321.
| Moderate thermal stress causes active and immediate expulsion of photosynthetically damaged zooxanthellae (Symbiodinium) from corals.Crossref | GoogleScholarGoogle Scholar | 25493938PubMed |
Gates, R. D., Baghdasarian, G., and Muscatine, L. (1992). Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. The Biological Bulletin 182, 324–332.
| Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching.Crossref | GoogleScholarGoogle Scholar | 29304594PubMed |
Goreau, T. F. (1959). The physiology of skeleton formation in corals. I. A method for measuring the rate of calcium deposition by corals under different conditions. The Biological Bulletin 116, 59–75.
| The physiology of skeleton formation in corals. I. A method for measuring the rate of calcium deposition by corals under different conditions.Crossref | GoogleScholarGoogle Scholar |
Goreau, T. F., and Goreau, N. I. (1959). The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef. The Biological Bulletin 117, 239–250.
| The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef.Crossref | GoogleScholarGoogle Scholar |
Hill, R., and Ralph, P. J. (2007). Post-bleaching viability of expelled zooxanthellae from the scleractinian coral Pocillopora damicornis. Marine Ecology Progress Series 352, 137–144.
| Post-bleaching viability of expelled zooxanthellae from the scleractinian coral Pocillopora damicornis.Crossref | GoogleScholarGoogle Scholar |
Hoegh-Guldberg, O. (1999). Climate change, coral bleaching and the future of the world’s coral reefs. Marine and Freshwater Research 50, 839–866.
| Climate change, coral bleaching and the future of the world’s coral reefs.Crossref | GoogleScholarGoogle Scholar |
Hoegh-Guldberg, O., and Smith, G. J. (1989). The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. Journal of Experimental Marine Biology and Ecology 129, 279–303.
| The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana.Crossref | GoogleScholarGoogle Scholar |
Hughes, T. P., Baird, A. H., Bellwood, D. R., Card, M., Connolly, S. R., Folke, C., Grosberg, R., Hoegh-Guldberg, O., Jackson, J. B. C., Kleypas, J., Lough, J. M., Marshall, P., Nystrom, M., Palumbi, S. R., Pandolfi, J. M., Rosen, B., and Roughgarden, J. (2003). Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933.
| Climate change, human impacts, and the resilience of coral reefs.Crossref | GoogleScholarGoogle Scholar | 12920289PubMed |
Hughes, T. P., Kerry, J. T., Álvarez-Noriega, M., Álvarez-Romero, J. G., Anderson, K. D., Baird, A. H., Babcock, R. C., Beger, M., Bellwood, D. R., Berkelmans, R., Bridge, T. C., Butler, I. R., Byrne, M., Cantin, N. E., Comeau, S., Connolly, S. R., Cumming, G. S., Dalton, S. J., Diaz-Pulido, G., Eakin, C. M., Figueira, W. F., Gilmour, J. P., Harrison, H. B., Heron, S. F., Hoey, A. S., Hobbs, J.-P. A., Hoogenboom, M. O., Kennedy, E. V., Kuo, C.-y., Lough, J. M., Lowe, R. J., Liu, G., McCulloch, M. T., Malcolm, H. A., McWilliam, M. J., Pandolfi, J. M., Pears, R. J., Pratchett, M. S., Schoepf, V., Simpson, T., Skirving, W. J., Sommer, B., Torda, G., Wachenfeld, D. R., Willis, B. L., and Wilson, S. K. (2017). Global warming and recurrent mass bleaching of corals. Nature 543, 373–377.
| Global warming and recurrent mass bleaching of corals.Crossref | GoogleScholarGoogle Scholar | 28300113PubMed |
Jeffrey, S. W., and Humphrey, G. F. (1975). New spectrophotometric equations for determining chlorophylls a, b, c1, and c2 in higher plants, algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen 167, 191–194.
| New spectrophotometric equations for determining chlorophylls a, b, c1, and c2 in higher plants, algae and natural phytoplankton.Crossref | GoogleScholarGoogle Scholar |
Johannes, R. E., and Wiebe, W. J. (1970). Method for determination of coral tissue biomass and composition. Limnology and Oceanography 15, 822–824.
| Method for determination of coral tissue biomass and composition.Crossref | GoogleScholarGoogle Scholar |
Jokiel, P. L., and Coles, S. L. (1990). Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8, 155–162.
| Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature.Crossref | GoogleScholarGoogle Scholar |
Jones, R. J., Hoegh-Guldberg, O., Larkum, A. W. D., and Schreiber, U. (1998). Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant, Cell & Environment 21, 1219–1230.
| Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae.Crossref | GoogleScholarGoogle Scholar |
Kleppel, G. S., Dodge, R. E., and Reese, C. J. (1989). Changes in pigmentation associated with the bleaching of stony corals. Limnology and Oceanography 34, 1331–1335.
| Changes in pigmentation associated with the bleaching of stony corals.Crossref | GoogleScholarGoogle Scholar |
Leggat, W., Seneca, F., Wasmund, K., Ukani, L., Yellowlees, D., and Ainsworth, T. D. (2011). Differential responses of the coral host and their algal symbiont to thermal stress. PLoS One 6, e26687.
| Differential responses of the coral host and their algal symbiont to thermal stress.Crossref | GoogleScholarGoogle Scholar | 22039532PubMed |
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 |
Lesser, M. P. (2006). Oxidative stress in marine environments: Biochemistry and physiological ecology. Annual Review of Physiology 68, 253–278.
| Oxidative stress in marine environments: Biochemistry and physiological ecology.Crossref | GoogleScholarGoogle Scholar | 16460273PubMed |
Lesser, M. P. (2011). Coral bleaching: causes and mechanisms. In ‘Coral Reefs: An Ecosystem in Transition’. (Eds Z. Dubinsky and N. Stambler.) pp. 405–419. (Springer Netherlands: Dordrecht, Netherlands.)
Lichocka, M., and Schmelzer, E. (2014). Subcellular localization experiments and FRET-FLIM measurements in plants. Bio-Protocol 4, 1–12.
| Subcellular localization experiments and FRET-FLIM measurements in plants.Crossref | GoogleScholarGoogle Scholar |
Middlebrook, R., Hoegh-Guldberg, O., and Leggat, W. (2008). The effect of thermal history on the susceptibility of reef-building corals to thermal stress. The Journal of Experimental Biology 211, 1050–1056.
| The effect of thermal history on the susceptibility of reef-building corals to thermal stress.Crossref | GoogleScholarGoogle Scholar | 18344478PubMed |
Muscatine, L., and Porter, J. W. (1977). Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27, 454–460.
| Reef corals: mutualistic symbioses adapted to nutrient-poor environments.Crossref | GoogleScholarGoogle Scholar |
Obura, D. O. (2009). Reef corals bleach to resist stress. Marine Pollution Bulletin 58, 206–212.
| Reef corals bleach to resist stress.Crossref | GoogleScholarGoogle Scholar | 18996547PubMed |
Ogawa, D., Bobeszko, T., Ainsworth, T. D., and Leggat, W. (2013). The combined effects of temperature and CO2 leas to altered gene expression in the Acropora aspera. Coral Reefs 32, 895–907.
| The combined effects of temperature and CO2 leas to altered gene expression in the Acropora aspera.Crossref | GoogleScholarGoogle Scholar |
Parry, M. L., Canziani, O. F., Palutikof, J. P., van der Linden, P. J., and Hanson, C. E. (2007). ‘Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, 2007.’ (Cambridge University Press: Cambridge, UK)
Sampayo, E. M., Ridgway, T., Bongaerts, P., and Hoegh-Guldberg, O. (2008). Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proceedings of the National Academy of Sciences of the United States of America 105, 10444–10449.
| Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type.Crossref | GoogleScholarGoogle Scholar | 18645181PubMed |
Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 22930834PubMed |
Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K. B., Tignor, M., and Miller, H. L. (2007). ‘Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, 2007.’ (Cambridge University Press: Cambridge, UK.)
Stambler, N. (2010). Coral symbiosis under stress. In ‘Symbioses and Stress: Joint Ventures in Biology’. (Eds J. Seckbach and M. Grube.) pp. 197–224. (Springer Netherlands: Dordrecht, Netherlands.)
Stat, M., Loh, W. K. W., LaJeunesse, T. C., Hoegh-Guldberg, O., and Carter, D. A. (2009). Stability of coral–endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28, 709–713.
| Stability of coral–endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef.Crossref | GoogleScholarGoogle Scholar |
Stimson, J., and Kinzie, R. A. (1991). The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. Journal of Experimental Marine Biology and Ecology 153, 63–74.
| The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions.Crossref | GoogleScholarGoogle Scholar |
Strong, A. E., Arzayus, F., Skirving, W., and Heron, S. F. (2013). Identifying coral bleaching remotely via coral reef watch – improved integration and implications for changing climate. In ‘Coral Reefs and Climate Change: Science and Management’. (Eds J. T. Phinney, O. Hoegh-Guldberg, J. Kleypas, W. Skirving, and A. Strong.) pp. 163–180. (American Geophysical Union: Washington, DC, USA.)
Strychar, K. B., Sammarco, P. W., and Piva, T. J. (2004). Apoptotic and necrotic stages of Symbiodinium (Dinophyceae) cell death activity: bleaching of soft and scleractinian corals. Phycologia 43, 768–777.
| Apoptotic and necrotic stages of Symbiodinium (Dinophyceae) cell death activity: bleaching of soft and scleractinian corals.Crossref | GoogleScholarGoogle Scholar |
Titlyanov, E., Titlyanova, T., Leletkin, V., Tsukahara, J., Van Woesik, R., and Yamazato, K. (1996). Degradation of zooxanthellae and regulation of their density in hermatypic corals. Marine Ecology Progress Series 139, 167–178.
| Degradation of zooxanthellae and regulation of their density in hermatypic corals.Crossref | GoogleScholarGoogle Scholar |
van Hooidonk, R., Maynard, J. A., and Planes, S. (2013). Temporary refugia for coral reefs in a warming world. Nature Climate Change 3, 508–511.
| Temporary refugia for coral reefs in a warming world.Crossref | GoogleScholarGoogle Scholar |
Warner, M. E., Fitt, W. K., and Schmidt, G. W. (1996). The effects of elevated temperature in the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant, Cell & Environment 19, 291–299.
| The effects of elevated temperature in the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach.Crossref | GoogleScholarGoogle Scholar |
Weis, V. M. (2008). Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. The Journal of Experimental Biology 211, 3059–3066.
| Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis.Crossref | GoogleScholarGoogle Scholar | 18805804PubMed |
Yellowlees, D., Rees, T. A. V., and Leggat, W. (2008). Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell & Environment 31, 679–694.
| Metabolic interactions between algal symbionts and invertebrate hosts.Crossref | GoogleScholarGoogle Scholar |
