Differential thermal tolerance between algae and corals may trigger the proliferation of algae in coral reefs.
Red Sea
heatwaves
thermal limits
thermal vulnerability
turf algae
Journal
Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746
Informations de publication
Date de publication:
08 2020
08 2020
Historique:
received:
07
05
2019
revised:
10
04
2020
accepted:
13
04
2020
pubmed:
5
5
2020
medline:
27
11
2020
entrez:
5
5
2020
Statut:
ppublish
Résumé
Marine heatwaves can lead to rapid changes in entire communities, including in the case of shallow coral reefs the potential overgrowth of algae. Here we tested experimentally the differential thermal tolerance between algae and coral species from the Red Sea through the measurement of thermal performance curves and the assessment of thermal limits. Differences across functional groups (algae vs. corals) were apparent for two key thermal performance metrics. First, two reef-associated algae species (Halimeda tuna and Turbinaria ornata) had higher lethal thermal limits than two coral species (Pocillopora verrucosa and Stylophora pistillata) conferring those species of algae with a clear advantage during heatwaves by surpassing the thermal threshold of coral survival. Second, the coral species had generally greater deactivation energies for net and gross primary production rates compared to the algae species, indicating greater thermal sensitivity in corals once the optimum temperature is exceeded. Our field surveys in the Red Sea reefs before and after the marine heatwave of 2015 show a change in benthic cover mainly in the southern reefs, where there was a decrease in coral cover and a concomitant increase in algae abundance, mainly turf algae. Our laboratory and field observations indicate that a proliferation of algae might be expected on Red Sea coral reefs with future ocean warming.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
4316-4327Subventions
Organisme : King Abdullah University of Science and Technology
Pays : International
Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Adey, W. H. (1998). Review-coral reefs: Algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. Journal of Phycology, 34(3), 393-406. https://doi.org/10.1046/j.1529-8817.1998.340393.x
Aichelman, H. E., Zimmerman, R. C., & Barshis, D. J. (2019). Adaptive signatures in thermal performance of the temperate coral Astrangia poculata. Journal of Experimental Biology, 222(5), jeb189225. https://doi.org/10.1242/jeb.189225
Amrhein, V., Greenland, S., & McShane, B. (2019). Scientists rise up against statistical significance. Nature, 567(7748), 305-307. https://doi.org/10.1038/d41586-019-00857-9
Anderson, B. C. (2006). Response of tropical marine macroalgae to thermal stress. Master thesis, Florida Atlantic University.
Arias-Ortiz, A., Serrano, O., Masqué, P., Lavery, P. S., Mueller, U., Kendrick, G. A., … Duarte, C. M. (2018). A marine heatwave drives massive losses from the world's largest seagrass carbon stocks. Nature Climate Change, 8(4), 338-344. https://doi.org/10.1038/s41558-018-0096-y
Aronson, R. B., & Precht, W. F. (2001). White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia, 460(1), 25-38. https://doi.org/10.1023/A:1013103928980
Bender, D., Diaz-Pulido, G., & Dove, S. (2014). Warming and acidification promote cyanobacterial dominance in turf algal assemblages. Marine Ecology Progress Series, 517, 271-284. https://doi.org/10.3354/meps11037
Bender-Champ, D., Diaz-Pulido, G., & Dove, S. (2017). Effects of elevated nutrients and CO2 emission scenarios on three coral reef macroalgae. Harmful Algae, 65, 40-51. https://doi.org/10.1016/j.hal.2017.04.004
Bridge, T. C. L., Ferrari, R., Bryson, M., Hovey, R., Figueira, W. F., Williams, S. B., … Byrne, M. (2014). Variable responses of benthic communities to anomalously warm sea temperatures on a high-latitude coral reef. PLoS ONE, 9(11), e113079. https://doi.org/10.1371/journal.pone.0113079
Brown, K. T., Bender-Champ, D., Kenyon, T. M., Rémond, C., Hoegh-Guldberg, O., & Dove, S. (2019). Temporal effects of ocean warming and acidification on coral-algal competition. Coral Reefs, 38(2), 297-309. https://doi.org/10.1007/s00338-019-01775-y
Bruno, J. F., Sweatman, H., Precht, W. F., Selig, E. R., & Schutte, V. G. W. (2009). Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology, 90(6), 1478-1484. https://doi.org/10.1890/08-1781.1
Cantin, N. E., Cohen, A. L., Karnauskas, K. B., Tarrant, A. M., & McCorkle, D. C. (2010). Ocean warming slows coral growth in the Central Red Sea. Science, 329(5989), 322-325. https://doi.org/10.1126/science.1190182
Chaidez, V., Dreano, D., Agusti, S., Duarte, C. M., & Hoteit, I. (2017). Decadal trends in Red Sea maximum surface temperature. Scientific Reports, 7(1), 8144. https://doi.org/10.1038/s41598-017-08146-z
Coles, S. L., & Brown, B. E. (2003). Coral bleaching-capacity for acclimatization and adaptation. Advances in Marine Biology, 46, 183-223.
Coles, S. L., & Riegl, B. M. (2013). Thermal tolerances of reef corals in the Gulf: A review of the potential for increasing coral survival and adaptation to climate change through assisted translocation. Marine Pollution Bulletin, 72(2), 323-332. https://doi.org/10.1016/j.marpolbul.2012.09.006
Coumou, D., & Rahmstorf, S. (2012). A decade of weather extremes. Nature Climate Change, 2(7), 491-496. https://doi.org/10.1038/NCLIMATE1452
Eakin, C. M., Morgan, J. A., Heron, S. F., Smith, T. B., Liu, G., Alvarez-Filip, L., … Yusuf, Y. (2010). Caribbean corals in crisis: Record thermal stress, bleaching, and mortality in 2005. PLoS ONE, 5(11), e13969. https://doi.org/10.1371/journal.pone.0013969
Ellis, J. I., Jamil, T., Anlauf, H., Coker, D. J., Curdia, J., Hewitt, J., … Hoteit, I. (2019). Multiple stressor effects on coral reef ecosystems. Global Change Biology, 25(12), 4131-4146. https://doi.org/10.1111/gcb.14819
Filbee-Dexter, K., Feehan, C. J., & Scheibling, R. E. (2016). Large-scale degradation of a kelp ecosystem in an ocean warming hotspot. Marine Ecology Progress Series, 543, 141-152. https://doi.org/10.3354/meps11554
Frölicher, T. L., Fischer, E. M., & Gruber, N. (2018). Marine heatwaves under global warming. Nature, 560(7718), 360-364. https://doi.org/10.1038/s41586-018-0383-9
García, F. C., Bestion, E., Warfield, R., & Yvon-Durocher, G. (2018). Changes in temperature alter the relationship between biodiversity and ecosystem functioning. Proceedings of the National Academy of Sciences of the United States of America, 115(43), 10989-10994. https://doi.org/10.1073/pnas.1805518115
Gegner, H. M., Rädecker, N., Ochsenkühn, M., Barreto, M. M., Ziegler, M., Reichert, J., … Voolstra, C. R. (2019). High levels of floridoside at high salinity link osmoadaptation with bleaching susceptibility in the cnidarian-algal endosymbiosis. Biology Open, 8(12), bio045591. https://doi.org/10.1242/bio.045591
Giomi, F., Barausse, A., Duarte, C. M., Booth, J., Agusti, S., Saderne, V., … Fusi, M. (2019). Oxygen supersaturation protects coastal marine fauna from ocean warming. Science Advances, 5(9), eaax1814. https://doi.org/10.1126/sciadv.aax1814
Gómez-Lemos, L. A., Doropoulos, C., Bayraktarov, E., & Diaz-Pulido, G. (2018). Coralline algal metabolites induce settlement and mediate the inductive effect of epiphytic microbes on coral larvae. Scientific Reports, 8(1), 1-11. https://doi.org/10.1038/s41598-018-35206-9
Graham, N. A. J., Jennings, S., MacNeil, M. A., Mouillot, D., & Wilson, S. K. (2015). Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature, 518(7537), 94-97. https://doi.org/10.1038/nature14140
Halsey, L. G. (2019). The reign of the p-value is over: What alternative analyses could we employ to fill the power vacuum? Biology Letters, 15(5), 20190174. https://doi.org/10.1098/rsbl.2019.0174
Harrington, L., Fabricius, K., De'ath, G., & Negri, A. (2004). Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecology, 85(12), 3428-3437. https://doi.org/10.1890/04-0298
Hoegh-Guldberg, O. (1999). Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research, 50(8), 839-866. https://doi.org/10.1071/mf99078
Hothorn, T., Bretz, F., & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal, 50(3), 346-363. https://doi.org/10.1002/bimj.200810425
Huey, R. B., & Kingsolver, J. G. (1989). Evolution of thermal sensitivity of ectotherm performance. Trends in Ecology & Evolution, 4(5), 131-135. https://doi.org/10.1016/0169-5347(89)90211-5
Hughes, D. J., Alderdice, R., Cooney, C., Kühl, M., Pernice, M., Voolstra, C. R., & Suggett, D. J. (2020). Coral reef survival under accelerating ocean deoxygenation. Nature Climate Change, 10(4), 296-307. https://doi.org/10.1038/s41558-020-0737-9
Hughes, T. P. (1994). Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral-reef. Science, 265(5178), 1547-1551. https://doi.org/10.1126/science.265.5178.1547
Hughes, T. P., Baird, A. H., Bellwood, D. R., Card, M., Connolly, S. R., Folke, C., … Roughgarden, J. (2003). Climate change, human impacts, and the resilience of coral reefs. Science, 301(5635), 929-933. https://doi.org/10.1126/science.1085046
Hughes, T. P., Graham, N. A. J., Jackson, J. B. C., Mumby, P. J., & Steneck, R. S. (2010). Rising to the challenge of sustaining coral reef resilience. Trends in Ecology & Evolution, 25(11), 633-642. https://doi.org/10.1016/j.tree.2010.07.011
Hughes, T. P., Kerry, J. T., Álvarez-Noriega, M., Álvarez-Romero, J. G., Anderson, K. D., Baird, A. H., … Wilson, S. K. (2017). Global warming and recurrent mass bleaching of corals. Nature, 543(7645), 373-377. https://doi.org/10.1038/nature21707
Hughes, T. P., Kerry, J. T., Baird, A. H., Connolly, S. R., Dietzel, A., Eakin, C. M., … Torda, G. (2018). Global warming transforms coral reef assemblages. Nature, 556(7702), 492-496. https://doi.org/10.1038/s41586-018-0041-2
Jaap, W. C., Szmant, A., Jaap, K., Dupont, J., Clarke, R., Somerfield, P., … Kellison, G. T. (2008). A perspective on the biology of Florida Keys coral reefs. In B. M. Riegl & R. E. Dodge (Eds.), Coral reefs of the USA (pp. 75-125). Dordrecht, the Netherlands: Springer Netherlands.
Jokiel, P. L., & Coles, S. L. (1977). Effects of temperature on the mortality and growth of Hawaiian reef corals. Marine Biology, 43(3), 201-208. https://doi.org/10.1007/BF00402312
Kattan, A., Coker, D. J., & Berumen, M. L. (2017). Reef fish communities in the central Red Sea show evidence of asymmetrical fishing pressure. Marine Biodiversity, 47(4), 1227-1238. https://doi.org/10.1007/s12526-017-0665-8
Kingsolver, J. G. (2009). The well-temperatured biologist. The American Naturalist, 174(6), 755-768. https://doi.org/10.1086/648310
Knowlton, N., Lang, J. C., & Keller, B. D. (1990). Case study of natural population collapse: Post-hurricane predation on Jamaican staghorn corals. Smithsonian Contributions to the Marine Sciences, 31, 1-25. https://doi.org/10.5479/si.01960768.31.11
Koch, M. S., George, B., Cliff, R., & Xing-Hai, Z. (2012). Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology, 19(1), 103-132. https://doi.org/10.1111/j.1365-2486.2012.02791.x
Kohler, K. E., & Gill, S. M. (2006). Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computers & Geosciences, 32(9), 1259-1269. https://doi.org/10.1016/j.cageo.2005.11.009
Kühl, M., Cohen, Y., Dalsgaard, T., Jørgensen, B. B., & Revsbech, N. P. (1995). Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Marine Ecology Progress Series, 117(1/3), 159-172. JSTOR.
Kürten, B., Khomayis, H. S., Devassy, R., Audritz, S., Sommer, U., Struck, U., … Al-Aidaroos, A. M. (2015). Ecohydrographic constraints on biodiversity and distribution of phytoplankton and zooplankton in coral reefs of the Red Sea, Saudi Arabia. Marine Ecology, 36(4), 1195-1214. https://doi.org/10.1111/maec.12224
Loreau, M., & Hector, A. (2001). Partitioning selection and complementarity in biodiversity experiments. Nature, 412(6842), 72-76. https://doi.org/10.1038/35083573
Marbà, N., & Duarte, C. M. (2010). Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Global Change Biology, 16(8), 2366-2375. https://doi.org/10.1111/j.1365-2486.2009.02130.x
Marbà, N., Jorda, G., Agusti, S., Girard, C., & Duarte, C. M. (2015). Footprints of climate change on Mediterranean Sea biota. Global Change and the Future Ocean, 56. https://doi.org/10.3389/fmars.2015.00056
McCook, L., Jompa, J., & Diaz-Pulido, G. (2001). Competition between corals and algae on coral reefs: A review of evidence and mechanisms. Coral Reefs, 19(4), 400-417. https://doi.org/10.1007/s003380000129
McMurray, S. E., Blum, J. E., Leichter, J. J., & Pawlik, J. R. (2011). Bleaching of the giant barrel sponge Xestospongia muta in the Florida Keys. Limnology and Oceanography, 56(6), 2243-2250. https://doi.org/10.4319/lo.2011.56.6.2243
Monroe, A. A., Ziegler, M., Roik, A., Röthig, T., Hardenstine, R. S., Emms, M. A., … Berumen, M. L. (2018). In situ observations of coral bleaching in the central Saudi Arabian Red Sea during the 2015/2016 global coral bleaching event. PLoS ONE, 13(4), e0195814. https://doi.org/10.1371/journal.pone.0195814
Nelson, H. R., & Altieri, A. H. (2019). Oxygen: The universal currency on coral reefs. Coral Reefs, 38(2), 177-198. https://doi.org/10.1007/s00338-019-01765-0
Normile, D. (2016). El Niño's warmth devastating reefs worldwide. Science, 352(6281), 15-16. https://doi.org/10.1126/science.352.6281.15
Ochsenkühn, M. A., Röthig, T., D'Angelo, C., Wiedenmann, J., & Voolstra, C. R. (2017). The role of floridoside in osmoadaptation of coral-associated algal endosymbionts to high-salinity conditions. Science Advances, 3(8), e1602047. https://doi.org/10.1126/sciadv.1602047
Oliver, E. C. J., Benthuysen, J. A., Bindoff, N. L., Hobday, A. J., Holbrook, N. J., Mundy, C. N., & Perkins-Kirkpatrick, S. E. (2017). The unprecedented 2015/16 Tasman Sea marine heatwave. Nature Communications, 8, 16101. https://doi.org/10.1038/ncomms16101
Oliver, E. C. J., Donat, M. G., Burrows, M. T., Moore, P. J., Smale, D. A., Alexander, L. V., … Wernberg, T. (2018). Longer and more frequent marine heatwaves over the past century. Nature Communications, 9, 1324. https://doi.org/10.1038/s41467-018-03732-9
Osman, E. O., Smith, D. J., Ziegler, M., Kürten, B., Conrad, C., El-Haddad, K. M., … Suggett, D. J. (2018). Thermal refugia against coral bleaching throughout the northern Red Sea. Global Change Biology, 24(2), e474-e484. https://doi.org/10.1111/gcb.13895
Padfield, D., Lowe, C., Buckling, A., Ffrench-Constant, R., Jennings, S., Shelley, F., … Yvon-Durocher, G. (2017). Metabolic compensation constrains the temperature dependence of gross primary production. Ecology Letters, 20(10), 1250-1260. https://doi.org/10.1111/ele.12820
Padfield, D., Yvon-Durocher, G., Buckling, A., Jennings, S., & Yvon-Durocher, G. (2016). Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton. Ecology Letters, 19(2), 133-142. https://doi.org/10.1111/ele.12545
Phelps, C. M., Boyce, M. C., & Huggett, M. J. (2017). Future climate change scenarios differentially affect three abundant algal species in southwestern Australia. Marine Environmental Research, 126, 69-80. https://doi.org/10.1016/j.marenvres.2017.02.008
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team. (2015). nlme: Linear and nonlinear mixed effects models. Retrieved from http://CRAN.R-project.org/package=nlme
Prathep, A., Wichachucherd, B., & Thongroy, P. (2007). Spatial and temporal variation in density and thallus morphology of Turbinaria ornata in Thailand. Aquatic Botany, 86(2), 132-138. https://doi.org/10.1016/j.aquabot.2006.09.011
Raitsos, D. E., Pradhan, Y., Brewin, R. J. W., Stenchikov, G., & Hoteit, I. (2013). Remote sensing the phytoplankton seasonal succession of the Red Sea. PLoS ONE, 8(6), e64909. https://doi.org/10.1371/journal.pone.0064909
Riegl, B. M., Johnston, M., Purkis, S., Howells, E., Burt, J., Steiner, S. C. C., … Bauman, A. (2018). Population collapse dynamics in Acropora downingi, an Arabian/Persian Gulf ecosystem-engineering coral, linked to rising temperature. Global Change Biology, 24(6), 2447-2462. https://doi.org/10.1111/gcb.14114
Riegl, B. M., Purkis, S. J., Al-Cibahy, A. S., Al-Harthi, S., Grandcourt, E., Al-Sulaiti, K., … Abdel-Moati, A. M. (2012). Coral bleaching and mortality thresholds in the SE gulf: Highest in the world. In B. M. Riegl & S. J. Purkis (Eds.), Coral reefs of the gulf: Adaptation to climatic extremes (pp. 95-105). Dordrecht, the Netherlands: Springer Netherlands.
Ritz, C., Baty, F., Streibig, J. C., & Gerhard, D. (2015). Dose-response analysis using R. PLoS ONE, 10(12), e0146021. https://doi.org/10.1371/journal.pone.0146021
Roberts, M. B., Jones, G. P., McCormick, M. I., Munday, P. L., Neale, S., Thorrold, S., … Berumen, M. L. (2016). Homogeneity of coral reef communities across 8 degrees of latitude in the Saudi Arabian Red Sea. Marine Pollution Bulletin, 105(2), 558-565. https://doi.org/10.1016/j.marpolbul.2015.11.024
Roff, G., Doropoulos, C., Zupan, M., Rogers, A., Steneck, R. S., Golbuu, Y., & Mumby, P. J. (2015). Phase shift facilitation following cyclone disturbance on coral reefs. Oecologia, 178(4), 1193-1203. https://doi.org/10.1007/s00442-015-3282-x
Savva, I., Bennett, S., Roca, G., Jordà, G., & Marbà, N. (2018). Thermal tolerance of Mediterranean marine macrophytes: Vulnerability to global warming. Ecology and Evolution, 8(23), 12032-12043. https://doi.org/10.1002/ece3.4663
Sheppard, C., Price, A., & Roberts, C. (1992). Marine ecology of the Arabian region: Patterns and processes in extreme tropical environments. Academic Press.
Silbiger, N. J., Goodbody-Gringley, G., Bruno, J. F., & Putnam, H. M. (2019). Comparative thermal performance of Orbicella franksi at its latitudinal range limits. BioRxiv. https://doi.org/10.1101/583294
Strong, A. E., Arzayus, F., Skirving, W., & Heron, S. F. (2006). Identifying coral bleaching remotely via coral reef watch - improved integration and implications for changing climate. In J. T. Phinney, O. Hoegh-Guldberg, J. Kleypas, W. Skirving, & A. Strong (Eds.), Coral reefs and climate change: Science and management. Coastal and Estuarine Studies (Vol. 61, pp. 163-180). Washington, DC: American Geophysical Union.
Thomas, M. K., Kremer, C. T., Klausmeier, C. A., & Litchman, E. (2012). A global pattern of thermal adaptation in marine phytoplankton. Science, 338(6110), 1085-1088. https://doi.org/10.1126/science.1224836
Tilman, D., Reich, P. B., Knops, J., Wedin, D., Mielke, T., & Lehman, C. (2001). Diversity and productivity in a long-term grassland experiment. Science, 294(5543), 843-845. https://doi.org/10.1126/science.1060391
Weeks, S. J., Anthony, K. R. N., Bakun, A., Feldman, G. C., & Hoegh-Guldberg, O. (2008). Improved predictions of coral bleaching using sea- sonal baselines and higher spatial resolution. Limnology and Oceanography, 53, 1369-1375.
Wellington, G. M., Glynn, P. W., Strong, A. E., Navarrete, S. A., Wieters, E., & Hubbard, D. (2001). Crisis on coral reefs linked to climate change. Eos, Transactions American Geophysical Union, 82(1), 1-5. https://doi.org/10.1029/01EO00001
Wernberg, T., Bennett, S., Babcock, R. C., de Bettignies, T., Cure, K., Depczynski, M., … Wilson, S. (2016). Climate-driven regime shift of a temperate marine ecosystem. Science, 353(6295), 169-172. https://doi.org/10.1126/science.aad8745
Wickham, H. (2009). ggplot2: Elegant graphics for data analysis. Springer-Verlag. Retrieved from https://www.springer.com/gp/book/9780387981413