Moberg, F. & Folke, C. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29, 215–233 (1999).
Google Scholar
Woodhead, A. J., Hicks, C. C., Norström, A. V., Williams, G. J. & Graham, N. A. J. Coral reef ecosystem services in the Anthropocene. Funct. Ecol. 33, 1023–1034 (2019).
Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82 (2017).
Google Scholar
Hughes, T. P., Kerry, J. T. & Simpson, T. Large-scale bleaching of corals on the Great Barrier Reef. Ecology 99, 501 (2017).
Google Scholar
Anthony, K. R. N., Kline, D. I., Diaz-Pulido, G., Dove, S. & Hoegh-Guldberg, O. Ocean acidification causes bleaching and productivity loss in coral reef builders. PNAS 105, 17442–17446 (2008).
Google Scholar
Courtial, L., Roberty, S., Shick, J. M., Houlbrèque, F. & Ferrier-Pagès, C. Interactive effects of ultraviolet radiation and thermal stress on two reef-building corals. Limnol. Oceanogr. 62, 1000–1013 (2017).
Google Scholar
Jessen, C. et al. In-situ effects of eutrophication and overfishing on physiology and bacterial diversity of the Red Sea Coral Acropora hemprichii. PLoS ONE 8, e62091 (2013).
Google Scholar
Jessen, C., Roder, C., Villa Lizcano, J. F., Voolstra, C. R. & Wild, C. In-situ effects of simulated overfishing and eutrophication on benthic coral reef algae growth, succession, and composition in the Central Red Sea. PLoS ONE 8, e66992 (2013).
Google Scholar
Fabricius, K. E. Effects of terrestrial runoff on the ecology of corals and coral reefs: Review and synthesis. Mar. Pollut. Bull. 50, 125–146 (2005).
Google Scholar
Hughes, T. P. et al. Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933 (2003).
Google Scholar
Fabricius, K. E., Cséke, S., Humphrey, C. & De’ath, G. Does trophic status enhance or reduce the thermal tolerance of scleractinian corals? A review, experiment and conceptual framework. PLoS ONE 8, e54399 (2013).
Google Scholar
McLachlan, R. H., Price, J. T., Solomon, S. L. & Grottoli, A. G. Thirty years of coral heat-stress experiments: A review of methods. Coral Reefs 39, 885–902 (2020).
Google Scholar
Fabricius, K. E. Factors determining the resilience of coral reefs to eutrophication: A review and conceptual model. In Coral Reefs: An Ecosystem in Transition (eds Dubinsky, Z. & Stambler, N.) (Springer, 2011).
Tilstra, A. et al. Light induced intraspecific variability in response to thermal stress in the hard coral Stylophora pistillata. PeerJ. https://doi.org/10.7717/PEERJ.3802/ (2017).
Google Scholar
Connolly, S. R., Lopez-Yglesias, M. A. & Anthony, K. R. N. Food availability promotes rapid recovery from thermal stress in a scleractinian coral. Coral Reefs 31, 951–960 (2012).
Google Scholar
Coles, S. L. & Brown, B. E. Coral bleaching—Capacity for acclimatization and adaptation. Adv. Mar. Biol. 46, 183 (2003).
Google Scholar
Rosenberg, E., Koren, O., Reshef, L., Efrony, R. & Zilber-Rosenberg, I. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5, 355–362 (2007).
Google Scholar
Szmant, A. M. Nutrient enrichment on coral reefs: Is it a major cause of coral reef decline? Estuaries 25, 743–766 (2002).
Google Scholar
Atkinson, M. J., Carlson, B. & Crow, G. L. Coral growth in high-nutrient, low-pH seawater: A case study of corals cultured at the Waikiki Aquarium, Honolulu, Hawaii. Coral Reefs 14, 215–223 (1995).
Google Scholar
Bongiorni, L., Shafir, S., Angel, D. & Rinkevich, B. Survival, growth and gonad development of two hermatypic corals subjected to in situ fish-farm nutrient enrichment. Mar. Ecol. Prog. Ser. 253, 137–144 (2003).
Google Scholar
Grigg, R. W. Coral reefs in an urban embayment in Hawaii: A complex case history controlled by natural and anthropogenic stress. Coral Reefs 14, 253–266 (1995).
Google Scholar
Fabricius, K. E. & De’ath, G. Identifying ecological change and its causes: A case study on coral reefs. Ecol. Appl. 14, 1448–1465 (2004).
Google Scholar
Ferrier-Pagès, C., Gattuso, J. P., Dallot, S. & Jaubert, J. Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata. Coral Reefs 19, 103–113 (2000).
Google Scholar
Rosset, S., Wiedenmann, J., Reed, A. J. & D’Angelo, C. Phosphate deficiency promotes coral bleaching and is reflected by the ultrastructure of symbiotic dinoflagellates. Mar. Pollut. Bull. 118, 180–187 (2017).
Google Scholar
Ban, S. S., Graham, N. A. J. & Connolly, S. R. Evidence for multiple stressor interactions and effects on coral reefs. Glob. Change Biol. 20, 681–697 (2014).
Google Scholar
Wiedenmann, J. et al. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat. Clim. Change 3, 160–164 (2012).
Google Scholar
Rädecker, N. et al. Heat stress destabilizes symbiotic nutrient cycling in corals. PNAS. https://doi.org/10.1073/pnas.2022653118 (2021).
Google Scholar
LaJeunesse, T. C. et al. Systematic revision of symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580 (2018).
Google Scholar
Falkowski, P. G., Dubinsky, Z., Muscatine, L. & McCloskey, L. Population control in symbiotic corals—Ammonium ions and organic materials maintain the density of zooxanthellae. Bioscience 43, 606–611 (1993).
Google Scholar
Muscatine, L. & Pool, R. R. Regulation of numbers of intracellular algae. Proc. R. Soc. Lond. Ser. B Biol. Sci. 204, 131–139 (1979).
Google Scholar
Muller-Parker, G., D’Elia, C. F. & Cook, C. B. Interactions between corals and their symbiotic algae. Coral Reefs Anthr. https://doi.org/10.1007/978-94-017-7249-5_5 (2015).
Google Scholar
Rädecker, N., Pogoreutz, C., Voolstra, C. R., Wiedenmann, J. & Wild, C. Nitrogen cycling in corals: The key to understanding holobiont functioning? Trends Microbiol. 23, 490–497 (2015).
Google Scholar
Steinberg, R. K., Dafforn, K. A., Ainsworth, T. & Johnston, E. L. Know thy anemone: A review of threats to octocorals and anemones and opportunities for their restoration. Front. Mar. Sci. 7, 590 (2020).
Google Scholar
Inoue, S., Kayanne, H., Yamamoto, S. & Kurihara, H. Spatial community shift from hard to soft corals in acidified water. Nat. Clim. Change 3, 683–687 (2013).
Google Scholar
Wild, C. & Naumann, M. S. Effect of active water movement on energy and nutrient acquisition in coral reef-associated benthic organisms. PNAS 110, 8767–8768 (2013).
Google Scholar
Fox, H. E., Pet, J. S., Dahuri, R. & Caldwell, R. L. Recovery in rubble fields: Long-term impacts of blast fishing. Mar. Pollut. Bull. 46, 1024–1031 (2003).
Google Scholar
Benayahu, Y. & Loya, Y. Settlement and recruitment of a soft coral: Why is Xenia macrospiculata a successful colonizer? Bull. Mar. Sci. 36, 177–188 (1985).
Norström, A. V., Nyström, M., Lokrantz, J. & Folke, C. Alternative states on coral reefs: Beyond coral-macroalgal phase shifts. Mar. Ecol. Prog. Ser. 376, 293–306 (2009).
Google Scholar
Reverter, M., Helber, S. B., Rohde, S., De Goeij, J. M. & Schupp, P. J. Coral reef benthic community changes in the Anthropocene: Biogeographic heterogeneity, overlooked configurations, and methodology. Glob. Change Biol. 28, 1956–1971 (2022).
Google Scholar
Karcher, D. B. et al. Nitrogen eutrophication particularly promotes turf algae in coral reefs of the central Red Sea. PeerJ 2020, 1–25 (2020).
El-Khaled, Y. C. et al. Nitrogen fixation and denitrification activity differ between coral- and algae-dominated Red Sea reefs. Sci. Rep. 11, 1–15 (2021).
Google Scholar
Ruiz-Allais, J. P., Benayahu, Y. & Lasso-Alcalá, O. M. The invasive octocoral Unomia stolonifera (Alcyonacea, Xeniidae) is dominating the benthos in the Southeastern Caribbean Sea. Mem. la Fund La Salle Ciencias Nat. 79, 63–80 (2021).
Ruiz Allais, J. P., Amaro, M. E., McFadden, C. S., Halász, A. & Benayahu, Y. The first incidence of an alien soft coral of the family Xeniidae in the Caribbean, an invasion in eastern Venezuelan coral communities. Coral Reefs 33, 287 (2014).
Google Scholar
Baum, G., Januar, I., Ferse, S. C. A., Wild, C. & Kunzmann, A. Abundance and physiology of dominant soft corals linked to water quality in Jakarta Bay, Indonesia. PeerJ 2016, 1–29 (2016).
Menezes, N. M. et al. New non-native ornamental octocorals threatening a South-west Atlantic reef. J. Mar. Biol. Assoc. U.K. https://doi.org/10.1017/S0025315421000849 (2022).
Google Scholar
Mantelatto, M. C., da Silva, A. G., dos Louzada, T. S., McFadden, C. S. & Creed, J. C. Invasion of aquarium origin soft corals on a tropical rocky reef in the southwest Atlantic. Brazil. Mar. Pollut. Bull. 130, 84–94 (2018).
Google Scholar
Simancas-Giraldo, S. M. et al. Photosynthesis and respiration of the soft coral Xenia umbellata respond to warming but not to organic carbon eutrophication. PeerJ 9, e11663 (2021).
Google Scholar
Vollstedt, S., Xiang, N., Simancas-Giraldo, S. M. & Wild, C. Organic eutrophication increases resistance of the pulsating soft coral Xenia umbellata to warming. PeerJ 2020, 1–16 (2020).
Thobor, B. et al. The pulsating soft coral Xenia umbellata shows high resistance to warming when nitrate concentrations are low. Sci. Rep. https://doi.org/10.1038/s41598-022-21110-w (2022).
Google Scholar
Costa, O. S., Leão, Z. M. A. N., Nimmo, M. & Attrill, M. J. Nutrification impacts on coral reefs from northern Bahia, Brazil. Hydrobiologia 440, 307–315 (2000).
Google Scholar
Fleury, B. G., Coll, J. C., Tentori, E., Duquesne, S. & Figueiredo, L. Effect of nutrient enrichment on the complementary (secondary) metabolite composition of the soft coral Sarcophyton ebrenbergi (Cnidaria: Octocorallia: Alcyonaceae) of the Great Barrier Reef. Mar. Biol. 136, 63–68 (2000).
Google Scholar
Bednarz, V. N., Naumann, M. S., Niggl, W. & Wild, C. Inorganic nutrient availability affects organic matter fluxes and metabolic activity in the soft coral genus Xenia. J. Exp. Biol. 215, 3672–3679 (2012).
Google Scholar
Bruno, J. F., Petes, L. E., Harvell, C. D. & Hettinger, A. Nutrient enrichment can increase the severity of coral diseases. Ecol. Lett. 6, 1056–1061 (2003).
Google Scholar
Ezzat, L., Maguer, J.-F.F., Grover, R. & Ferrier-Pagès, C. Limited phosphorus availability is the Achilles heel of tropical reef corals in a warming ocean. Sci. Rep. 6, 1–11 (2016).
Google Scholar
Tanaka, Y., Grottoli, A. G., Matsui, Y., Suzuki, A. & Sakai, K. Effects of nitrate and phosphate availability on the tissues and carbonate skeleton of scleractinian corals. Mar. Ecol. Prog. Ser. 570, 101–112 (2017).
Google Scholar
Liu, G., Strong, A. E., Skirving, W. & Arzayus, L. F. Overview of NOAA coral reef watch program’s near-real time satellite global coral bleaching monitoring activities. In Proc. 10th International Coral Reef Symposium, 1783–1793 (2006).
Bellworthy, J. & Fine, M. Beyond peak summer temperatures, branching corals in the Gulf of Aqaba are resilient to thermal stress but sensitive to high light. Coral Reefs 36, 1071–1082 (2017).
Google Scholar
Rex, A., Montebon, F. & Yap, H. T. Metabolic responses of the scleractinian coral Porites cylindrica Dana to water motion. I. Oxygen flux studies. J. Exp. Mar. Biol. Ecol. 186, 33–52 (1995).
Google Scholar
Long, M. H., Berg, P., de Beer, D. & Zieman, J. C. In situ coral reef oxygen metabolism: An eddy correlation study. PLoS ONE 8, e58581 (2013).
Google Scholar
Fabricius, K. E. & Klumpp, D. W. Widespread mixotrophy in reef-inhabiting soft corals: The influence of depth, and colony expansion and contraction on photosynthesis. Mar. Ecol. Prog. Ser. 125, 195–204 (1995).
Google Scholar
Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).
Google Scholar
Raimonet, M., Guillou, G., Mornet, F. & Richard, P. Macroalgae δ15N values in well-mixed estuaries: Indicator of anthropogenic nitrogen input or macroalgae metabolism? Estuar. Coast. Shelf Sci. 119, 126–138 (2013).
Google Scholar
Furla, P., Galgani, I., Durand, I. & Allemand, D. Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J. Exp. Biol. 203, 3445–3457 (2000).
Google Scholar
Hughes, A. D., Grottoli, A. G., Pease, T. K. & Matsui, Y. Acquisition and assimilation of carbon in non-bleached and bleached corals. Mar. Ecol. Prog. Ser. 420, 91–101 (2010).
Google Scholar
Rau, G. H., Takahashi, T. & Des Marais, D. J. Latitudinal variations in plankton delta C-13—Implications for CO2 and productivity in past oceans. Nature 341, 516–518 (1989).
Google Scholar
McMahon, K. W., Hamady, L. L. & Thorrold, S. R. A review of ecogeochemistry approaches to estimating movements of marine animals. Limnol. Oceanogr. 58, 697–714 (2013).
Google Scholar
Muscatine, L., Porter, J. W. & Kaplan, I. R. Resource partitioning by reef corals as determined from stable isotope composition. Mar. Biol. 100, 185–193 (1989).
Google Scholar
Swart, P. K. et al. The isotopic composition of respired carbon dioxide in scleractinian corals: Implications for cycling of organic carbon in corals. Geochim. Cosmochim. Acta 69, 1495–1509 (2005).
Google Scholar
Rodrigues, L. J. & Grottoli, A. G. Calcification rate and the stable carbon, oxygen, and nitrogen isotopes in the skeleton, host tissue, and zooxanthellae of bleached and recovering Hawaiian corals. Geochim. Cosmochim. Acta 70, 2781–2789 (2006).
Google Scholar
Grottoli, A. G. & Rodrigues, L. J. Bleached Porites compressa and Montipora capitata corals catabolize δ13C-enriched lipids. Coral Reefs 30, 687–692 (2011).
Google Scholar
Levas, S. J., Grottoli, A. G., Hughes, A., Osburn, C. L. & Matsui, Y. Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral porites lobata: Implications for resilience in mounding corals. PLoS ONE 8, 32–35 (2013).
Google Scholar
Schoepf, V. et al. Annual coral bleaching and the long-term recovery capacity of coral. Proc. R. Soc. B Biol. Sci. 282, 20151887 (2015).
Google Scholar
Lesser, M. P. et al. Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa. Mar. Ecol. Prog. Ser. 346, 143–152 (2007).
Google Scholar
Carpenter, E. J., Harvey, H. R., Brian, F. & Capone, D. G. Biogeochemical tracers of the marine cyanobacterium Trichodesmium. Deep Sea Res. I Oceanogr. Res. Pap. 44, 27–38 (1997).
Google Scholar
Lachs, L. et al. Effects of tourism-derived sewage on coral reefs: Isotopic assessments identify effective bioindicators. Mar. Pollut. Bull. 148, 85–96 (2019).
Google Scholar
Kürten, B. et al. Influence of environmental gradients on C and N stable isotope ratios in coral reef biota of the Red Sea, Saudi Arabia. J. Sea Res. 85, 379–394 (2014).
Google Scholar
Core Team, R. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).
Wickham, H. et al. Welcome to the Tidyverse. J. Open Source Softw. 4, 1686 (2019).
Google Scholar
Kassambara, A. ggpubr: ‘ggplot2’ Based Publication Ready Plots. R Package Version 0.4.0 (2020).
Kassambara, A. rstatix: Pipe-Friendly Framework for Basic Statistical Tests. R Package Version 0.7.0 (2021).
Contreras-Silva, A. I. et al. A meta-analysis to assess long-term spatiotemporal changes of benthic coral and macroalgae cover in the Mexican Caribbean. Sci. Rep. 10, 1–12 (2020).
Google Scholar
Ledlie, M. H. et al. Phase shifts and the role of herbivory in the resilience of coral reefs. Coral Reefs 26, 641–653 (2007).
Google Scholar
Kuffner, I. B. & Toth, L. T. A geological perspective on the degradation and conservation of western Atlantic coral reefs. Conserv. Biol. 30, 706–715 (2016).
Google Scholar
Hughes, T. P. Catastrophes, phase shifts, and large-scale degradation of a Caribbean Coral Reef. Science 265, 1547–1551 (1994).
Google Scholar
de Bakker, D. M., Meesters, E. H., Bak, R. P. M., Nieuwland, G. & van Duyl, F. C. Long-term shifts in coral communities on shallow to deep reef slopes of Curaçao and Bonaire: Are there any winners? Front. Mar. Sci. 3, 247 (2016).
Google Scholar
Mergner, H. & Svoboda, A. Productivity and seasonal changes in selected reef areas in the Gulf of Aqaba (Red Sea). Helgoländer Meeresun. 30, 383–399 (1977).
Google Scholar
Schlichter, D., Svoboda, A. & Kremer, B. P. Functional autotrophy of Heteroxenia fuscescens (Anthozoa: Alcyonaria): Carbon assimilation and translocation of photosynthates from symbionts to host. Mar. Biol. 78, 29–38 (1983).
Google Scholar
Al-Sofyani, A. A. & Niaz, G. R. A comparative study of the components of the hard coral Seriatopora hystrix and the soft coral Xenia umbellata along the Jeddah coast, Saudi Arabia. Rev. Biol. Mar. Oceanogr. 42, 207–219 (2007).
Google Scholar
McCloskey, L. R., Wethey, D. S. & Porter, J. W. Measurement and interpretation of photosynthesis and respiration in reef corals. In Coral Reefs: Research Methods (eds Stoddart, D. R. & Johannes, R. E.) 379–396 (United Nations Educational, Scientific and Cultural Organization, 1978).
Baker, D. M., Freeman, C. J., Wong, J. C. Y., Fogel, M. L. & Knowlton, N. Climate change promotes parasitism in a coral symbiosis. ISME J. 12, 921–930 (2018).
Google Scholar
Hoegh-Guldberg, O. & Smith, G. J. 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. J. Exp. Mar. Biol. Ecol. 129, 279–303 (1989).
Google Scholar
Iglesias-Prieto, R., Matta, J. L., Robins, W. A. & Trench, R. K. Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc. Natl. Acad. Sci. 89, 10302–10305 (1992).
Google Scholar
Béraud, E., Gevaert, F., Rottier, C. & Ferrier-Pagès, C. The response of the scleractinian coral Turbinaria reniformis to thermal stress depends on the nitrogen status of the coral holobiont. J. Exp. Biol. 216, 2665–2674 (2013).
Kremien, M., Shavit, U., Mass, T. & Genin, A. Benefit of pulsation in soft corals. Proc. Natl. Acad. Sci. U.S.A. 110, 8978–8983 (2013).
Google Scholar
Grover, R. et al. Coral uptake of inorganic phosphorus and nitrogen negatively affected by simultaneous changes in temperature and pH. PLoS ONE 6, 1–10 (2011).
Cardini, U. et al. Microbial dinitrogen fixation in coral holobionts exposed to thermal stress and bleaching. Environ. Microbiol. 18, 2620–2633 (2016).
Google Scholar
Cardini, U. et al. Functional significance of dinitrogen fixation in sustaining coral productivity under oligotrophic conditions. Proc. R. Soc. B Biol. Sci. 282, 20152257 (2015).
Google Scholar
Santos, H. F. et al. Climate change affects key nitrogen-fixing bacterial populations on coral reefs. ISME J. 8, 2272–2279 (2014).
Google Scholar
Tilstra, A. et al. Relative diazotroph abundance in symbiotic red sea corals decreases with water depth. Front. Mar. Sci. 6, 372 (2019).
Google Scholar
Klinke, A. et al. Impact of phosphate enrichment on the susceptibility of the pulsating soft coral Xenia umbellata to ocean warming. Front. Mar. Sci. 9, 1026321 (2022).
Google Scholar
Rädecker, N. et al. Heat stress reduces the contribution of diazotrophs to coral holobiont nitrogen cycling. ISME J. https://doi.org/10.1038/s41396-021-01158-8 (2021).
Google Scholar
Swart, P. K., Saied, A. & Lamb, K. Temporal and spatial variation in the δ15N and δ13C of coral tissue and zooxanthellae in Montastraea faveolata collected from the Florida reef tract. Limnol. Oceanogr. 50, 1049–1058 (2005).
Google Scholar
Grottoli, A. G., Tchernov, D. & Winters, G. Physiological and biogeochemical responses of super-corals to thermal stress from the Northern Gulf of Aqaba, Red Sea. Front. Mar. Sci. 4, 215 (2017).
Google Scholar
Dubinsky, Z. & Stambler, N. Marine pollution and coral reefs. Glob. Change Biol. 2, 511–526 (1996).
Google Scholar
Loya, Y., Lubinevsky, H., Rosenfeld, M. & Kramarsky-Winter, E. Nutrient enrichment caused by in situ fish farms at Eilat, Red Sea is detrimental to coral reproduction. Mar. Pollut. Bull. 49, 344–353 (2004).
Google Scholar
Costa, O. S., Nimmo, M. & Attrill, M. J. Coastal nutrification in Brazil: A review of the role of nutrient excess on coral reef demise. J. S. Am. Earth Sci. 25, 257–270 (2008).
Google Scholar
Tait, D. R. et al. The influence of groundwater inputs and age on nutrient dynamics in a coral reef lagoon. Mar. Chem. 166, 36–47 (2014).
Google Scholar
Guan, Y., Hohn, S., Wild, C. & Merico, A. Vulnerability of global coral reef habitat suitability to ocean warming, acidification and eutrophication. Glob. Change Biol. 26, 5646–5660 (2020).
Google Scholar
Hall, E. R. et al. Eutrophication may compromise the resilience of the Red Sea coral Stylophora pistillata to global change. Mar. Pollut. Bull. 131, 701–711 (2018).
Google Scholar
Naumann, M. S. et al. Organic matter release by dominant hermatypic corals of the Northern Red Sea. Coral Reefs 29, 649–659 (2010).
Google Scholar
Wild, C. et al. Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428, 66–70 (2004).
Google Scholar
Source: Ecology - nature.com