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研究生: 高洛德
Rodrigo Enrique Carballo Bolanos
論文名稱: 墾丁地區密集迷紋珊瑚(Leptoria phrygia)和鐘形微孔珊瑚(Porites lutea)對不同溫度環境的生理差異及馴化過程
Physiological differences and acclimatisation processes in two scleractinian corals: Leptoria phrygia and Porites lutea, from two sites with contrasting temperature regimes in Kenting National Park, southern Taiwan
指導教授: 陳昭倫
Chen, Chao-Lun
學位類別: 博士
Doctor
系所名稱: 生命科學系
Department of Life Science
論文出版年: 2020
畢業學年度: 108
語文別: 英文
論文頁數: 134
中文關鍵詞: 珊瑚
英文關鍵詞: Leptoria phrygia, acclimatisation, high temperature variability, Kenting, Porites lutea, Durusdinium, Cladocopium
DOI URL: http://doi.org/10.6345/NTNU202000365
論文種類: 學術論文
相關次數: 點閱:119下載:18
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  • The frequency and severity of global bleaching events are increasing, due to the rise of anthropogenic CO2 in the atmosphere. As our oceans keep warming up, understanding the mechanisms driving thermal tolerance in reef-building corals is of outstanding importance. In Kenting National Park, southern Taiwan, there is a ‘Variable Site’ (VS) that is influenced by the constant hot-water effluent from a nuclear power plant outlet and temperatures during the summer can be 3 °C higher that at any other site within Kenting. It is also influenced by a monthly upwelling that makes seawater temperature to fluctuate up to 8 °C in one day. In this dissertation, I collected samples of Leptoria phrygia from the VS and from a ‘Stable Site’ (SS) that is not affected by high temperature or high temperature fluctuations within Kenting and compared physiological parameters to elucidate the mechanisms this species has to survive in the VS (Chapters II and III). Results suggest that L. phrygia is a species that presents multi-symbiont association and inter-colony variation in SS: most colonies associated with Cladocopium spp. (stress-sensitive), some colonies had co-dominance between Durusdinium glynnii and Cladocopium spp., and very few associated only with D. glynnii (stress-resistant). Meanwhile in the VS, L. phrygia associated all year long with D. glynnii (>90% dominance). I found out that only those colonies with a co-dominance exhibited temporal variation, and I hypothesize that those co-dominant colonies might be able to survive future scenarios of climate change by modifying the relative abundance of both symbionts. If the environment becomes stressful, it becomes Durusdinium-dominant similar to the current situation in the VS.
    Furthermore, I performed a reciprocal transplantation experiment with L. phrygia and Porites lutea between both sites, to understand the acclimatisation processes to thermal stress (in the summer) and to high temperature variation throughout the year (Chapter IV). Results indicate that both species have different mechanisms to resist stress and to acclimatise to their new environment. Leptoria phrygia is dependent on the different Symbiodiniaceae association and is able to acclimatise faster than P. lutea, but only if it presents co-dominance of Cladocopium spp. and Durusdinium spp. within the colony. If they are >90% Cladocopium-dominant, then they cannot survive high temperatures in the summer in VS. In contrast, P. lutea acclimatise to the new environment slower and modified both partners physiology to confront changes in the environment. The results of this dissertation increase our knowledge on coral physiology and specifically on the differences between species. Even though both species are able to acclimatise to rapid changes in climate using different mechanisms, it is imperative to change completely our societal dependence on fossil fuels, in order to address the root causes of climate change.

    Table of Contents List of Tables……………………………………………………….…..ix List of Figures…………………………………………………………...x CHAPTER 1: General introduction………….………………….….1 Background………………………………………………………….….1 Mechanisms to survive thermal stress………………………….……3 1.Thermally tolerant endosymbionts…………………….…………3 2.Acclimatisation (phenotypic plasticity)……………………..…….6 2.1 Thermal stress acclimatisation………………….…….7 2.2 Acclimatisation to high temperature variability..............9 3.Adaptation……………………...………………………………12 4.Heterotrophy (Mixotrophy)………………………………………15 Research overview……………………………………………………16 CHAPTER 2: Temporal variation and photochemical efficiency of species in Symbiodiniaceae associated with coral Leptoria phrygia (Scleractinia; Merulinidae) exposed to contrasting temperature regimes……..…………………………………………20 Abstract……………………………………………………...…………20 Introduction…………………………………………………………….22 Materials and methods……………………………………………….27 Study sites and temperature data………………………………….27 Sample collection, photochemical efficiency and preservation……..29 Laboratory analyses………………………………...…………….30 Surface area……….……………………………………………..30 Symbiont density……………….…………………………………31 Chlorophyll a concentration………………………………………..31 Molecular analysis……….………………………………………..32 DNA extraction……………………………………………..32 Quantitative PCR (qPCR)…………..………………………32 Symbiont identification – (DGGE)…………………………..33 Statistical analysis…………….…………………………………..34 Results…………………………………………………………………35 Seawater temperature differences between sites………………….35 Symbiodiniaceae association……………..………………………36 Correlation between Durusdinium spp. and temperature…………..39 Physiological parameters……………..…………………………..40 Discussion……………………………………………………………..41 Supplemental Information……………………………………………49 CHAPTER 3: Differences in δ13C and δ15N isotopic niches of Leptoria phrygia associated with Cladocopium spp. or Durusdinium spp. symbionts……………………………………..51 Abstract………………………………………………………………..51 Introduction……………………………………………………………52 Materials and methods…………………………………………….…56 Study sites and coral sample collection………..…………….…….56 Coral sample preparation……………..…………………….…….57 Stable isotope analysis…………………………….………….…..59 Molecular analysis: DNA extraction and qPCR…………………….60 Statistical analysis………………………………….……………..60 Results…………………………………………………………………62 Temperature differences between sites………………...………….62 Strength of the symbiotic relationship within C-dominant and D- dominant corals…………..…………………………..…………..62 Differences in isotopic niche, δ13C and δ15N between C- dominant and D-dominant corals……………………………………..………….63 Temporal variation in isotopic niche………………..…..…….……68 Correlation between δ13C/ δ15N and the percentage of Durusdinium spp………………………………..………………………..…….70 Discussion……………………………………………………………..71 Supplemental information……………………………………………75 CHAPTER 4: Acclimatisation processes in Leptoria phrygia and Porites lutea when transplanted to a habitat with different seawater temperature variability in southern Taiwan…...……78 Abstract…………………………………………………………...……78 Introduction…………………………………………………………….79 Materials and methods…………………………………….…………84 Study sites and temperature data……..………..…………………84 Experimental design……………………………………………....85 Photochemical efficiency………………………………………….87 Laboratory analyses……………………………………………....87 Surface area……….………………………………………87 Symbiont density……………….…………………………..88 Chlorophyll a concentration…………………………………88 Lipid concentration………………………………...……….89 Protein concentration……………………………………….89 Molecular analysis……….………………………………………..90 DNA extraction and qPCR………………………………….90 Statistical analysis………………………….……………………..90 Results…………………………………………………………………92 Seawater temperature differences between sites………………….92 QPCR……………………….……………………………………94 Mortality………………………………………………….……….94 Photochemical efficiency………………………………………….95 Symbiont density………………………..………………………..97 Chlorophyll a concentration……………….………………………99 Lipid concentration (algae and coral host fractions)………………100 Protein concentration (coral host fraction)……………………..…103 Discussion……………………………………………………………105 Supplemental information…………………………………………..110 CHAPTER 5: Conclusions………………………………….…….111 References………………………………………………..………….117

    Alamaru, A., Y. Loya, E. Brokovich, R. Yam, and A. Shemesh. 2009. Carbon and nitrogen utilization in two species of Red Sea corals along a depth gradient: Insights from stable isotope analysis of total organic material and lipids. Geochimica et Cosmochimica Acta 73:5333-5342.
    Anthony, K., L. K. Bay, R. Costanza, J. Firn, J. Gunn, P. Harrison, A. Heyward, P. Lundgren, D. Mead, and T. Moore. 2017. New interventions are needed to save coral reefs. Nature Ecology & Evolution 1:1420.
    Anthony, K., M. O. Hoogenboom, J. A. Maynard, A. G. Grottoli, and R. Middlebrook. 2009. Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Functional ecology 23:539-550.
    Anthony, K. R., S. R. Connolly, and O. Hoegh-Guldberg. 2007. Bleaching, energetics, and coral mortality risk: Effects of temperature, light, and sediment regime. Limnology and Oceanography 52:716-726.
    Anthony, K. R. N., and K. E. Fabricius. 2000. Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. Journal of Experimental Marine Biology and Ecology 252:221-253.
    Baker, A., T. McClanahan, C. Starger, and R. Boonstra. 2013a. Long-term monitoring of algal symbiont communities in corals reveals stability is taxon dependent and driven by site-specific thermal regime. Marine Ecology Progress Series 479:85-97.
    Baker, A. C. 2003. Flexibility and specificity in coral-agal symbiosis: diversity, ecology, and biogeogrpahy of Symbiodinium. Annual Reviews of Ecology, Evolution, and Systematics 34:661-689.
    Baker, D. M., J. P. Andras, A. G. Jordán-Garza, and M. L. Fogel. 2013b. Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades. The ISME Journal 7:1248-1251.
    Baker, D. M., C. J. Freeman, J. C. Wong, M. L. Fogel, and N. Knowlton. 2018. Climate change promotes parasitism in a coral symbiosis. The ISME Journal:1.
    Barkley, H. C., A. L. Cohen, N. R. Mollica, R. E. Brainard, H. E. Rivera, T. M. DeCarlo, G. P. Lohmann, E. J. Drenkard, A. E. Alpert, C. W. Young, B. Vargas-Ángel, K. C. Lino, T. A. Oliver, K. R. Pietro, and V. H. Luu. 2018. Repeat bleaching of a central Pacific coral reef over the past six decades (1960–2016). Communications Biology 1:177.
    Barshis, D. J., J. T. Ladner, T. A. Oliver, F. O. Seneca, N. Traylor-Knowles, and S. R. Palumbi. 2013. Genomic basis for coral resilience to climate change. Proceedings of the National Academy of Sciences 110:1387-1392.
    Barshis, D. J., J. H. Stillman, R. D. Gates, R. J. Toonen, L. W. Smith, and C. Birkeland. 2010. Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity? Molecular ecology 19:1705-1720.
    Bates, A. E., R. S. C. Cooke, M. I. Duncan, G. J. Edgar, J. F. Bruno, L. Benedetti-Cecchi, I. M. Côté, J. S. Lefcheck, M. J. Costello, N. Barrett, T. J. Bird, P. B. Fenberg, and R. D. Stuart-Smith. 2019. Climate resilience in marine protected areas and the ‘Protection Paradox’. Biological Conservation 236:305-314.
    Bates, D., M. Maechler, and B. Bolker. 2012. lme4: Linear mixed-effects models using S4 classes. R package version 0.999999-0. Vienna.
    Baumann, J., A. G. Grottoli, A. D. Hughes, and Y. Matsui. 2014. Photoautotrophic and heterotrophic carbon in bleached and non-bleached coral lipid acquisition and storage. Journal of Experimental Marine Biology and Ecology 461:469-478.
    Bay, L. K., J. Doyle, M. Logan, and R. Berkelmans. 2016. Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral. Royal Society open science 3:160322.
    Bay, R. A., and S. R. Palumbi. 2017. Transcriptome predictors of coral survival and growth in a highly variable environment. Ecology and evolution 7:4794-4803.
    Bay, R. A., N. H. Rose, C. A. Logan, and S. R. Palumbi. 2017. Genomic models predict successful coral adaptation if future ocean warming rates are reduced. Science Advances 3:e1701413.
    Bayraktarov, E., M. I. Saunders, S. Abdullah, M. Mills, J. Beher, H. P. Possingham, P. J. Mumby, and C. E. Lovelock. 2016. The cost and feasibility of marine coastal restoration. Ecological Applications 26:1055-1074.
    Bearhop, S., C. E. Adams, S. Waldron, R. A. Fuller, and H. Macleod. 2004. Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 73:1007-1012.
    Bellantuono, A. J., O. Hoegh-Guldberg, and M. Rodriguez-Lanetty. 2012. Resistance to thermal stress in corals without changes in symbiont composition. Proceedings of the Royal Society B: Biological Sciences 279:1100-1107.
    Bellwood, D. R., M. S. Pratchett, T. H. Morrison, G. G. Gurney, T. P. Hughes, J. G. Álvarez-Romero, J. C. Day, R. Grantham, A. Grech, A. S. Hoey, G. P. Jones, J. M. Pandolfi, S. B. Tebbett, E. Techera, R. Weeks, and G. S. Cumming. 2019. Coral reef conservation in the Anthropocene: Confronting spatial mismatches and prioritizing functions. Biological Conservation 236:604-615.
    Berkelmans, R., and M. J. H. van Oppen. 2006. The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proceedings of the Royal Society B: Biological Sciences 273:2305-2312.
    Beyer, H. L., E. V. Kennedy, M. Beger, C. A. Chen, J. E. Cinner, E. S. Darling, C. M. Eakin, R. D. Gates, S. F. Heron, N. Knowlton, D. O. Obura, S. R. Palumbi, H. P. Possingham, M. Puotinen, R. K. Runting, W. J. Skirving, M. Spalding, K. A. Wilson, S. Wood, J. E. Veron, and O. Hoegh-Guldberg. 2018. Risk-sensitive planning for conserving coral reefs under rapid climate change. Conservation Letters 11:e12587.
    Borell, E. M., and K. Bischof. 2008. Feeding sustains photosythetic quantum yield of a scleractinian coral during thermal stress. Oecologia 157:593-601.
    Borell, E. M., A. R. Yuliantri, K. Bischof, and C. Richter. 2008. The effect of heterotrophy on photosynthesis and tissue composition of two scleractinian corals under elevated temperature. Journal of Experimental Marine Biology and Ecology 364:116-123.
    Brown, B., R. Dunne, M. Warner, I. Ambarsari, W. Fitt, S. Gibb, and D. Cummings. 2000. Damage and recovery of Photosystem II during a manipulative field experiment on solar bleaching in the coral Goniastrea aspera. Marine Ecology Progress Series 195:117-124.
    Brown, B. E. 1997a. Adaptations of reef corals to physical environmental stress. Advances in Marine Biology 31:222-299.
    Brown, B. E. 1997b. Coral bleaching: causes and consequences. Coral Reefs 16:S129-S138.
    Brown, B. E., and A. R. Cossins. 2011. The potential for temperature acclimatisation of reef corals in the face of climate change. Pages 421-433 Coral Reefs: An Ecosystem in Transition. Springer.
    Brown, B. E., R. P. Dunne, I. Ambarsari, M. D. A. L. Tissier, and U. Satapoomin. 1999. Seasonal fluctuations in environmental factors and variations in symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species. Marine Ecology Progress Series 191:53-69.
    Brown, B. E., R. P. Dunne, A. J. Edwards, M. J. Sweet, and N. Phongsuwan. 2015. Decadal environmental ‘memory’in a reef coral? Marine Biology 162:479-483.
    Bruno, J. F., I. M. Côté, and L. T. Toth. 2019. Climate Change, Coral Loss, and the Curious Case of the Parrotfish Paradigm: Why Don't Marine Protected Areas Improve Reef Resilience? Annual Review of Marine Science 11:307-334.
    Bruno, J. F., and E. R. Selig. 2007. Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS One 2:e711.
    Buddemeier, R. W., and D. G. Fautin. 1993. Coral bleaching as an adaptive mechanism: a testable hypothesis. Bioscience 43:320-326.
    Burt, J. A., F. Paparella, N. Al-Mansoori, A. Al-Mansoori, and H. Al-Jailani. 2019. Causes and consequences of the 2017 coral bleaching event in the southern Persian/Arabian Gulf. Coral Reefs 38:567-589.
    Carballo-Bolaños, R., V. Denis, Y.-Y. Huang, S. Keshavmurthy, and C. A. Chen. 2019. Temporal variation and photochemical efficiency of species in Symbiodinaceae associated with coral Leptoria phrygia (Scleractinia; Merulinidae) exposed to contrasting temperature regimes. PLoS One 14:e0218801.
    Chakravarti, L. J., V. H. Beltran, and M. J. van Oppen. 2017. Rapid thermal adaptation in photosymbionts of reef‐building corals. Global change biology 23:4675-4688.
    Chan, W. Y., L. M. Peplow, P. Menéndez, A. A. Hoffmann, and M. J. H. van Oppen. 2018. Interspecific Hybridization May Provide Novel Opportunities for Coral Reef Restoration. Frontiers in Marine Science 5.
    Chen, C. A., K. K. Lam, Y. Nakano, and W.-S. Tsai. 2003. A stable association of the stress-tolerant zooxanthellae, Symbiodinium clade D, with the low-temperature-tolerant coral, Oulastrea crispata (Scleractinia: Faviidae) in subtropical non-reefal coral communities. Zoological Studies 42:540-550.
    Chen, C. A., J.-T. Wang, L.-S. Fang, and Y.-W. Yang. 2005. Fluctuating algal symbiont communities in Acropora palifera (Scleractinia: Acroporidae) in Taiwan. Marine Ecology Progress Series 295:113-121.
    Chiou, W. D., L. Z. Cheng, and H. C. Ou. 1993. Relationship between the dispersion of thermal effluent and the tidal current in the waters near the outlet of the third nuclear power plant in southern Taiwan. Journal of Fisheries Society of Taiwan 20:207-220.
    Cignoni, P., M. Callieri, M. Corsini, M. Dellepiane, F. Ganovelli, and G. Ranzuglia. 2008. Meshlab: an open-source mesh processing tool. Pages 129-136 in Eurographics Italian Chapter Conference.
    Coffroth, M. A., D. M. Poland, E. L. Petrou, D. A. Brazeau, and J. C. Holmberg. 2010. Environmental symbiont acquisition may not be the solution to warming sea for reef-building corals. PLoS One 5:e13258.
    Cohen, J. E. 1995. Population growth and earth's human carrying capacity. Science 269:341-346.
    Coles, S. L., K. D. Bahr, K. u. S. Rodgers, S. L. May, A. E. McGowan, A. Tsang, J. Bumgarner, and J. H. Han. 2018. Evidence of acclimatization or adaptation in Hawaiian corals to higher ocean temperatures. PeerJ 6:e5347.
    Coles, S. L., and B. E. Brown. 2003. Coral bleaching - capacity for acclimatization and adaptation. Advances in Marine Biology 46:183-223.
    Coles, S. L., and B. M. Riegl. 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 72:323-332.
    Cooper, T. F., R. Berkelmans, K. E. Ulstrup, S. Weeks, B. Radford, A. M. Jones, J. Doyle, M. Canto, R. A. O'Leary, and M. J. H. van Oppen. 2011. Environmental factors controlling the distribution of Symbiodinium harboured by the coral Acropora millepora on the Great Barrier Reef. PLoS One 6:e25536.
    Cunning, R., R. Silverstein, and A. Baker. 2015. Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change. Proceedings of the Royal Society of London B: Biological Sciences 282:20141725.
    Cunning, R., R. N. Silverstein, and A. C. Baker. 2017. Symbiont shuffling linked to differential photochemical dynamics of Symbiodinium in three Caribbean reef corals. Coral Reefs:1-8.
    Cziesielski, M. J., S. Schmidt‐Roach, and M. Aranda. 2019. The past, present, and future of coral heat stress studies. Ecology and evolution.
    D’Angelo, C., and J. Wiedenmann. 2014. Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Current Opinion in Environmental Sustainability 7:82-93.
    Darling, E. S., and I. M. Côté. 2018. Seeking resilience in marine ecosystems. Science 359:986-987.
    Davy, S. K., D. Allemand, and V. M. Weis. 2012. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76:229-261.
    De’ath, G., K. E. Fabricius, H. Sweatman, and M. Puotinen. 2012. The 27–year decline of coral cover on the Great Barrier Reef and its causes. Proceedings of the National Academy of Sciences 109:17995-17999.
    DeNiro, M. J., and S. Epstein. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42:495-506.
    Dixon, G. B., S. W. Davies, G. V. Aglyamova, E. Meyer, L. K. Bay, and M. V. Matz. 2015. Genomic determinants of coral heat tolerance across latitudes. Science 348:1460-1462.
    Douglas, A. E. 2003. Coral bleaching- how and why? Marine pollution bulletin 46:385-392.
    Dubinsky, Z., and N. Stambler. 1996. Marine pollution and coral reefs. Global change biology 2:511-526.
    Durante, M. K., I. B. Baums, D. E. Williams, S. Vohsen, and D. W. Kemp. 2019. What drives phenotypic divergence among coral clonemates of Acropora palmata? Molecular ecology 0.
    Eakin, C. M., H. P. A. Sweatman, and R. E. Brainard. 2019. The 2014–2017 global-scale coral bleaching event: insights and impacts. Coral Reefs 38:539-545.
    Edgar, G. J., R. D. Stuart-Smith, T. J. Willis, S. Kininmonth, S. C. Baker, S. Banks, N. S. Barrett, M. A. Becerro, A. T. Bernard, and J. Berkhout. 2014. Global conservation outcomes depend on marine protected areas with five key features. Nature 506:216.
    Edmunds, P. J., and R. D. Gates. 2008. Acclimatization in tropical reef corals. Marine Ecology Progress Series 361:307-310.
    Einbinder, S., T. Mass, E. Brokovich, Z. Dubinsky, J. Erez, and D. Tchernov. 2009. Changes in morphology and diet of the coral Stylophora pistillata along a depth gradient. Marine Ecology Progress Series 381:167-174.
    Eirin-Lopez, J. M., and H. M. Putnam. 2019. Marine Environmental Epigenetics. Annual Review of Marine Science 11:335-368.
    Fabricius, K. E. 2005. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Marine pollution bulletin 50:125-146.
    Fagoonee, I., H. B. Wilson, M. P. Hassell, and J. R. Turner. 1999. The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843-845.
    Fan, K. L. 1991. The thermal effluent problems of three nuclear power plants in Taiwan. Oceanogr. Ser. 54:309-403.
    Ferrara, G. B., B. Murgia, A. M. Parodi, L. Valisano, C. Cerrano, G. Palmisano, G. Bavestrello, and M. Sara. 2006a. The assessment of DNA from marine organisms via a modified salting-out protocol. Cell Mol Biol Lett 11:155-160.
    Ferrara, G. B., B. Murgia, A. M. Parodi, L. Valisano, C. Cerrano, G. Palmisano, G. Bavestrello, and M. Sara. 2006b. The assessment of DNA from marine organisms via a modified salting-out protocol. Cell Mol Biol Lett:150-160.
    Ferrier‐Pagès, C., and M. C. Leal. 2019. Stable isotopes as tracers of trophic interactions in marine mutualistic symbioses. Ecology and evolution 9:723-740.
    Fine, M., H. Gildor, and A. Genin. 2013. A coral reef refuge in the Red Sea. Global change biology 19:3640-3647.
    Fisch, J., C. Drury, E. K. Towle, R. N. Winter, and M. W. Miller. 2019. Physiological and reproductive repercussions of consecutive summer bleaching events of the threatened Caribbean coral Orbicella faveolata. Coral Reefs 38:863-876.
    Fisher, P. L., M. K. Malme, and S. Dove. 2012. The effect of temperature stress on coral-Symbiodinium associations containing distinct symbiont types. Coral Reefs 31:473-485.
    Fitt, W. K., B. E. Brown, M. E. Warner, and R. P. Dunne. 2001. Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51-65.
    Fitt, W. K., F. K. McFarland, M. E. Warner, and G. C. Chilcoat. 2000. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnology and Oceanography 45:677-685.
    Folch, J., M. Lees, and G. Sloane-Stanley. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. biol. Chem 226:497-509.
    Fox, M. D., A. L. Carter, C. B. Edwards, Y. Takeshita, M. D. Johnson, V. Petrovic, C. G. Amir, E. Sala, S. A. Sandin, and J. E. Smith. 2019. Limited coral mortality following acute thermal stress and widespread bleaching on Palmyra Atoll, central Pacific. Coral Reefs 38:701-712.
    Frade, P. R., P. Bongaerts, N. Englebert, A. Rogers, M. Gonzalez-Rivero, and O. Hoegh-Guldberg. 2018. Deep reefs of the Great Barrier Reef offer limited thermal refuge during mass coral bleaching. Nature Communications 9:3447.
    Frieler, K., M. Meinshausen, A. Golly, M. Mengel, K. Lebek, S. D. Donner, and O. Hoegh-Guldberg. 2012. Limiting global warming to 2 °C is unlikely to save most coral reefs. Nature Climate Change 3:165.
    Fry, B. 2006. Stable isotope ecology. Springer.
    Fry, B., and E. B. Sherr. 1989. δ 13 C measurements as indicators of carbon flow in marine and freshwater ecosystems. Pages 196-229 Stable isotopes in ecological research. Springer.
    Furla, P., I. Galgani, I. Durand, and D. Allemand. 2000. Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. Journal of Experimental Biology 203:3445-3457.
    Gardner, T. A., I. M. Côté, J. A. Gill, A. Grant, and A. R. Watkinson. 2003. Long-Term Region-Wide Declines in Caribbean Corals. Science 301:958-960.
    Glynn, P. 1993. Coral reef bleaching: ecological perspectives. Coral Reefs 12:1-17.
    Goreau, T. F., N. I. Goreau, and C. M. Yonge. 1971. Reef corals: Autotrophs or Heterotrophs? . The Biological Bulletin 141:247-260.
    Goulet, T. L. 2006. Most corals may not change their symbionts. Marine Ecology Progress Series 321:1-7.
    Graham, N. A., D. R. Bellwood, J. E. Cinner, T. P. Hughes, A. V. Norström, and M. Nyström. 2013. Managing resilience to reverse phase shifts in coral reefs. Frontiers in Ecology and the Environment 11:541-548.
    Grorud-Colvert, K., J. Claudet, B. N. Tissot, J. E. Caselle, M. H. Carr, J. C. Day, A. M. Friedlander, S. E. Lester, T. L. de Loma, D. Malone, and W. J. Walsh. 2014. Marine Protected Area Networks: Assessing Whether the Whole Is Greater than the Sum of Its Parts. PLoS One 9:e102298.
    Grottoli, A., and L. Rodrigues. 2011. Bleached Porites compressa and Montipora capitata corals catabolize δ13C-enriched lipids. Coral Reefs 30:687-692.
    Grottoli, A. G., L. J. Rodrigues, and J. E. Palardy. 2006. Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186-1189.
    Grottoli, A. G., M. E. Warner, S. J. Levas, M. D. Aschaffenburg, V. Schoepf, M. McGinley, J. Baumann, and Y. Matsui. 2014. The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Global change biology 20:3823-3833.
    Grover, R., J.-F. Maguer, D. Allemand, and C. Ferrier-Pages. 2003. Nitrate uptake in the scleractinian coral Stylophora pistillata. Limnology and Oceanography 48:2266-2274.
    Grover, R., J.-F. Maguer, D. Allemand, and C. Ferrier-Pagès. 2006. Urea uptake by the scleractinian coral Stylophora pistillata. Journal of Experimental Marine Biology and Ecology 332:216-225.
    Grover, R., J.-F. Maguer, D. Allemand, and C. Ferrier-Pagès. 2008. Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata. Journal of Experimental Biology 211:860-865.
    Grover, R., J.-F. Maguer, S. Reynaud-Vaganay, and C. Ferrier-Pages. 2002. Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammonium concentrations. Limnology and Oceanography 47:782-790.
    Guest, J. R., A. H. Baird, J. A. Maynard, E. Muttaqin, A. J. Edwards, S. J. Campbell, K. Yewdall, Y. A. Affendi, and L. M. Chou. 2012. Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS One 7:e33353.
    Harrison, H. B., M. Álvarez-Noriega, A. H. Baird, S. F. Heron, C. MacDonald, and T. P. Hughes. 2019. Back-to-back coral bleaching events on isolated atolls in the Coral Sea. Coral Reefs 38:713-719.
    Hartfield, G., J. Blunden, and D. S. Arndt. 2018. State of the Climate in 2017. Bulletin of the American Meteorological Society 99:Si-S310.
    Hawkins, T. D., and M. E. Warner. 2017. Warm preconditioning protects against acute heat-induced respiratory dysfunction and delays bleaching in a symbiotic sea anemone. Journal of Experimental Biology 220:969-983.
    Head, C. E. I., D. T. I. Bayley, G. Rowlands, R. C. Roche, D. M. Tickler, A. D. Rogers, H. Koldewey, J. R. Turner, and D. A. Andradi-Brown. 2019. Coral bleaching impacts from back-to-back 2015–2016 thermal anomalies in the remote central Indian Ocean. Coral Reefs 38:605-618.
    Heikoop, J., J. Dunn, M. Risk, T. Tomascik, H. Schwarcz, I. Sandeman, and P. Sammarco. 2000. δ15 N and δ13 C of coral tissue show significant inter-reef variation. Coral Reefs 19:189-193.
    Heikoop, J. M., J. J. Dunn, M. J. Risk, I. M. Sandeman, H. P. Schwartz, and N. Waltho. 1998. Relationship between light and the S15N of coral tissue: Examples from Jamaica and Zanzibar. Limnology and Oceanography 43:909-920.
    Hereford, J. 2009. A quantitative survey of local adaptation and fitness trade-offs. The American Naturalist 173:579-588.
    Heron, S. F., J. A. Maynard, R. Van Hooidonk, and C. M. Eakin. 2016. Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Scientific reports 6:38402.
    Hoegh-Guldberg, O. 1999. Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50:839-866.
    Hoegh-Guldberg, O. 2012. The adaptation of coral reefs to climate change: Is the Red Queen being outpaced? Scientia Marina 76:403-408.
    Hoegh-Guldberg, O., L. Hughes, S. Mclntyre, D. B. Lindenmayer, C. Parmesan, H. P. Possingham, and C. D. Thomas. 2008. Assisted colonization and rapid climate change. Science 321:345-346.
    Hoegh-Guldberg, O., E. V. Kennedy, H. L. Beyer, C. McClennen, and H. P. Possingham. 2018. Securing a long-term future for coral reefs. Trends in Ecology & Evolution.
    Hoegh-Guldberg, O., P. J. Mumby, A. J. Hooten, R. S. Steneck, P. Greenfield, E. Gomez, C. D. Harvell, P. F. Sale, A. J. Edwards, K. Caldeira, N. Knowlton, C. M. Eakin, R. Iglesias-Prieto, N. Muthiga, R. H. Bradbury, A. Dubi, and M. E. Hatziolos. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:1737-1742.
    Hoogenboom, M., C. Rottier, S. Sikorski, and C. Ferrier-Pagès. 2015. Among-species variation in the energy budgets of reef-building corals: scaling from coral polyps to communities. Journal of Experimental Biology 218:3866-3877.
    Houlbrèque, F., and C. Ferrier‐Pagès. 2009. Heterotrophy in tropical scleractinian corals. Biological Reviews 84:1-17.
    Howells, E. J., V. H. Beltrán, N. W. Larsen, L. K. Bay, B. L. Willis, and M. J. H. van Oppen. 2012. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Climate Change 2:116-120.
    Hsu, C.-M., S. Keshavmurthy, V. Dennis, C.-Y. Kuo, J.-T. Wang, P.-J. Meng, and C. A. Chen. 2012. Temporal and spatial variations of symbiont communities in catch bowl coral, Isopora palifera (Scleractinia; Acroporidae), at reefs in Kenting National Park, Taiwan. Zoological Studies 51:1343-1353
    Hughes, A., A. Grottoli, T. Pease, and Y. Matsui. 2010. Acquisition and assimilation of carbon in non-bleached and bleached corals. Marine Ecology Progress Series 420:91-101.
    Hughes, A. D., and A. G. Grottoli. 2013. Heterotrophic Compensation: A Possible Mechanism for Resilience of Coral Reefs to Global Warming or a Sign of Prolonged Stress? PLoS One 8:e81172.
    Hughes, T. P., K. D. Anderson, S. R. Connolly, S. F. Heron, J. T. Kerry, J. M. Lough, A. H. Baird, J. K. Baum, M. L. Berumen, T. C. Bridge, D. C. Claar, C. M. Eakin, J. P. Gilmour, N. A. J. Graham, H. Harrison, J.-P. A. Hobbs, A. S. Hoey, M. Hoogenboom, R. J. Lowe, M. T. McCulloch, J. M. Pandolfi, M. Pratchett, V. Schoepf, G. Torda, and S. K. Wilson. 2018a. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80-83.
    Hughes, T. P., A. H. Baird, D. R. Bellwood, M. Card, S. R. Connolly, C. Folke, R. Grosberg, O. Hoegh-Guldberg, J. B. C. Jackson, J. Kleypas, J. M. Lough, P. Marshall, M. Nyström, S. R. Palumbi, J. M. Pandolfi, B. Rosen, and J. Roughgarden. 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301:929-933.
    Hughes, T. P., M. L. Barnes, D. R. Bellwood, J. E. Cinner, G. S. Cumming, J. B. Jackson, J. Kleypas, I. A. Van De Leemput, J. M. Lough, and T. H. Morrison. 2017a. Coral reefs in the Anthropocene. Nature 546:82.
    Hughes, T. P., J. T. Kerry, M. Álvarez-Noriega, J. G. Álvarez-Romero, K. D. Anderson, A. H. Baird, R. C. Babcock, M. Beger, D. R. Bellwood, and R. Berkelmans. 2017b. Global warming and recurrent mass bleaching of corals. Nature 543:373-377.
    Hughes, T. P., J. T. Kerry, A. H. Baird, S. R. Connolly, A. Dietzel, C. M. Eakin, S. F. Heron, A. S. Hoey, M. O. Hoogenboom, and G. Liu. 2018b. Global warming transforms coral reef assemblages. Nature 556:492.
    Hughes, T. P., J. T. Kerry, S. R. Connolly, A. H. Baird, C. M. Eakin, S. F. Heron, A. S. Hoey, M. O. Hoogenboom, M. Jacobson, G. Liu, M. S. Pratchett, W. Skirving, and G. Torda. 2019. Ecological memory modifies the cumulative impact of recurrent climate extremes. Nature Climate Change 9:40-43.
    Hume, B. C., C. D'Angelo, E. G. Smith, J. R. Stevens, J. Burt, and J. Wiedenmann. 2015. Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in corals of the world's hottest sea, the Persian/Arabian Gulf. Scientific reports 5:8562.
    Hume, B. C. C., C. R. Voolstra, C. Arif, C. D’Angelo, J. A. Burt, G. Eyal, Y. Loya, and J. Wiedenmann. 2016. Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proceedings of the National Academy of Sciences 113:4416-4421.
    Jackson, A. L., R. Inger, A. C. Parnell, and S. Bearhop. 2011. Comparing isotopic niche widths among and within communities: SIBER–Stable Isotope Bayesian Ellipses in R. Journal of Animal Ecology 80:595-602.
    Jackson, J. B., M. X. Kirby, W. H. Berger, K. A. Bjorndal, L. W. Botsford, B. J. Bourque, R. H. Bradbury, R. Cooke, J. Erlandson, and J. A. Estes. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629-637.
    Jan, S., and C.-T. A. Chen. 2009. Potential biogeochemical effects from vigorous internal tides generated in Luzon Strait: A case study at the southernmost coast of Taiwan. Journal of Geophysical Research: Oceans 114:C04021.
    Jeffrey, S. t., and G. Humphrey. 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.
    Johannes, R. E., and W. J. Wiebe. 1970. Method for determination of coral tissue biomass and composition. Limnology and Oceanography:822-824.
    Jokiel, P. L. 2004. Temperature stress and coral bleaching. Pages 401-425 Coral health and disease. Springer.
    Jones, A., and R. Berkelmans. 2010 Potential costs of acclimatization to warmer climate: growth of a reef corals with heat tolerant vs. sensitive symbiont types. PLoS One 5:e10437.
    Jones, A. M., R. Berkelmans, M. J. H. van Oppen, J. C. Mieog, and W. Sinclair. 2008. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society B: Biological Sciences 275:1359-1365.
    Kaebnick, G. E., E. Heitman, J. P. Collins, J. A. Delborne, W. G. Landis, K. Sawyer, L. A. Taneyhill, and D. E. Winickoff. 2016. Precaution and governance of emerging technologies. Science 354:710-711.
    Kao, K.-W., S. Keshavmurthy, C.-H. Tsao, J.-T. Wang, and C. Allen. 2018. Repeated and Prolonged Temperature Anomalies Negate Symbiodiniaceae Genera Shuffling in the Coral Platygyra verweyi (Scleractinia; Merulinidae). Zoological Studies 57.
    Kemp, D. W., X. Hernandez-Pech, R. Iglesias-Prieto, W. K. Fitt, and G. W. Schmidt. 2014. Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event. Limnology and Oceanography 59:788-797.
    Kemp, D. W., D. J. Thornhill, R. D. Rotjan, R. Iglesias-Prieto, W. K. Fitt, and G. W. Schmidt. 2015. Spatially distinct and regionally endemic Symbiodinium assemblages in the threatened Caribbean reef-building coral Orbicella faveolata. Coral Reefs 34:535-547.
    Kenkel, C. D., and M. V. Matz. 2017. Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nature Ecology & Evolution 1:0014.
    Keshavmurthy, S., C.-M. Hsu, C.-Y. Kuo, P.-J. Meng, J.-T. Wang, and C. A. Chen. 2012 Symbiont communities and host genetic structure of the brain coral Platygyra verweyi, at the outlet of a nuclear power plant and adjacent areas. Molecular ecology 21:4393-4407.
    Keshavmurthy, S., C.-Y. Kuo, Y.-Y. Huang, R. Carballo-Bolaños, P.-J. Meng, J.-T. Wang, and C. A. Chen. 2019. Coral Reef Resilience in Taiwan: Lessons from Long-Term Ecological Research on the Coral Reefs of Kenting National Park (Taiwan). Journal of Marine Science and Engineering 7:388.
    Keshavmurthy, S., P.-J. Meng, J.-T. Wang, C.-Y. Kuo, S.-Y. Yang, C.-M. Hsu, C.-H. Gan, C.-F. Dai, and C. A. Chen. 2014. Can resistant coral-Symbiodinium associations enable coral communities to survive climate change? A study of a site exposed to long-term hot water input. Peer J 2:e327.
    Krueger, T., N. Horwitz, J. Bodin, M.-E. Giovani, S. Escrig, A. Meibom, and M. Fine. 2017. Common reef-building coral in the Northern Red Sea resistant to elevated temperature and acidification. Royal Society open science 4:170038.
    Ku‘ulei, S. R., K. D. Bahr, P. L. Jokiel, and A. R. Donà. 2017. Patterns of bleaching and mortality following widespread warming events in 2014 and 2015 at the Hanauma Bay Nature Preserve, Hawai ‘i. PeerJ 5:e3355.
    LaJeunesse, T. C. 2002. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology 141:387-400.
    LaJeunesse, T. C., J. E. Parkinson, P. W. Gabrielson, H. J. Jeong, J. D. Reimer, C. R. Voolstra, and S. R. Santos. 2018. Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts. Current Biology 28:2570-2580.e2576.
    LaJeunesse, T. C., D. T. Pettay, E. M. Sampayo, N. Phongsuwan, B. Brown, D. O. Obura, O. Hoegh-Guldberg, and W. K. Fitt. 2010a. Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. Journal of Biogeography 37:785-800.
    LaJeunesse, T. C., R. Smith, M. Walther, J. Pinzón, D. T. Pettay, M. McGinley, M. Aschaffenburg, P. Medina-Rosas, A. L. Cupul-Magaña, A. L. Pérez, H. Reyes-Bonilla, and M. E. Warner. 2010b. Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. Proceedings of the Royal Society B: Biological Sciences.
    Lajeunesse, T. C., R. T. Smith, J. Finney, and H. Oxenford. 2009. Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral 'bleaching' event. Proceedings of the Royal Society B: Biological Sciences 276:4139-4148.
    Layman, C. A., D. A. Arrington, C. G. Montaña, and D. M. Post. 2007. Can stable isotope ratios provide for community‐wide measures of trophic structure? Ecology 88:42-48.
    Lee, H.-J., S.-Y. Chao, K.-L. Fan, and T.-Y. Kuo. 1999. Tide-induced eddies and upwelling in a semi-enclosed basin: Nan Wan. Estuarine, Coastal and Shelf Science 49:775-787.
    Lee, H.-J., S.-Y. Chao, K.-L. Fan, Y.-H. Wang, and N.-H. Liang. 1997. Tidally induced upwelling in a semi-enclosed basin: Nan Wan Bay. Journal of Oceanography 53:467-480.
    Lesser, M. P. 2006. Oxidative stress in marine environments: biochemistry and physiological ecology. Annu. Rev. Physiol. 68:253-278.
    Levas, S., A. G. Grottoli, V. Schoepf, M. Aschaffenburg, J. Baumann, J. E. Bauer, and M. E. Warner. 2016. Can heterotrophic uptake of dissolved organic carbon and zooplankton mitigate carbon budget deficits in annually bleached corals? Coral Reefs 35:495-506.
    Levas, S. J., A. G. Grottoli, A. Hughes, C. L. Osburn, and Y. Matsui. 2013. 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:e63267.
    Levin, R. A., C. R. Voolstra, S. Agrawal, P. D. Steinberg, D. J. Suggett, and M. J. H. van Oppen. 2017. Engineering Strategies to Decode and Enhance the Genomes of Coral Symbionts. Frontiers in Microbiology 8.
    Lewis, C., K. L. Neely, and M. Rodriguez-Lanetty. 2019. Recurring episodes of thermal stress shift the balance from a dominant host-specialist to a background host-generalist zooxanthella in the threatened pillar coral, Dendrogyra cylindrus. Frontiers in Marine Science 6:1.
    Lien, Y.-T., S. Keshavmurthy, Y. Nakano, P. Sakanan, H. Huang, C.-M. Hsu, H. Fukami, Y. Yamashita, H. J. Hsieh, J.-T. Wang, and C. A. Chen. 2013. Host genetics and Symbiodinium D diversity in a stress-tolerant scleractinian coral, Oulastrea crispata, in the West Pacific. Marine Ecology Progress Series 473: 163-177.
    Lien, Y.-T., Y. Nakano, S. Plathong, H. Fukami, J.-T. Wang, and C. A. Chen. 2007. Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlying coral communities. Coral Reefs 26:35-44.
    Maier, C., M. Weinbauer, and J. Pätzold. 2010. Stable isotopes reveal limitations in C and N assimilation in the Caribbean reef corals Madracis auretenra, M. carmabi and M. formosa. Marine Ecology Progress Series 412:103-112.
    Mateo, M. A., O. Serrano, L. Serrano, and R. H. Michener. 2008. Effects of sample preparation on stable isotope ratios of carbon and nitrogen in marine invertebrates: implications for food web studies using stable isotopes. Oecologia 157:105-115.
    Mayfield, A. B., T.-Y. Fan, and C.-S. Chen. 2013. Physiological acclimation to elevated temperature in a reef-building coral from an upwelling environment. Coral Reefs 32:909-921.
    Maynard, J. A., K. R. N. Anthony, P. A. Marshall, and I. Masiri. 2008. Major bleaching events can lead to increased thermal tolerance in corals. Marine Biology.
    McClanahan, T. R., C. J. Starger, and A. C. Baker. 2015. Decadal changes in common reef coral populations and their associations with algal symbionts (Symbiodinium spp.). Marine ecology 36:1215-1229.
    McCloskey, L. R., L. Muscatine, and D. C. Smith. 1984. Production and respiration in the Red Sea coral <i>Stylophora pistillata</i> as a function of depth. Proceedings of the Royal Society of London. Series B. Biological Sciences 222:215-230.
    McCulloch, M., S. Fallon, T. Wyndham, E. Hendy, J. Lough, and D. Barnes. 2003. Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature 421:727.
    McCutchan Jr, J. H., W. M. Lewis Jr, C. Kendall, and C. C. McGrath. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378-390.
    Meng, P.-J., H.-J. Lee, J.-T. Wang, C.-C. Chen, H.-J. Lin, K. S. Tew, and W.-J. Hsieh. 2008. A long-term survey on anthropogenic impacts to the water quality of coral reefs, southern Taiwan. Environmental Pollution 156:76-75.
    Middlebrook, R., O. Hoegh-Guldberg, and W. Leggat. 2008. The effect of thermal history on the susceptibility of reef-building corals to thermal stress. Journal of Experimental Biology 211:1050-1056.
    Mieog, J. C., M. J. van Oppen, N. E. Cantin, W. T. Stam, and J. L. Olsen. 2007. Real-time PCR reveals a high incidence of Symbiodinium clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs 26:449-457.
    Mieog, J. C., M. J. H. van Oppen, R. Berkelmans, W. T. Stam, and J. L. Olsen. 2009. Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Molecular Ecology Resources 9:74-82.
    Minagawa, M., and E. Wada. 1984. Stepwise enrichment of 15N along food chains: Further evidence and the relation between δ15N and animal age. Geochimica et Cosmochimica Acta 48:1135-1140.
    Morikawa, M. K., and S. R. Palumbi. 2019. Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries. Proceedings of the National Academy of Sciences 116:10586-10591.
    Mumby, P. J., I. A. Elliott, C. M. Eakin, W. Skirving, C. B. Paris, H. J. Edwards, S. Enríquez, R. Iglesias‐Prieto, L. M. Cherubin, and J. R. Stevens. 2011. Reserve design for uncertain responses of coral reefs to climate change. Ecology letters 14:132-140.
    Muscatine, L. 1990. The role of symbiotic algae in carbon and energy flux in reef corals. Pages 75-87 in Z. Dubinsky, editor. Ecosystems of the world. Elsevier Science Publishing Company, The Nederlands.
    Muscatine, L., and C. D'elia. 1978. The uptake, retention, and release of ammonium by reef corals 1. Limnology and Oceanography 23:725-734.
    Muscatine, L., J. W. Porter, and I. R. Kaplan. 1989. Resource partitioning by reef corals as determined from stable isotope composition. Marine Biology 100:185-193.
    Muscatine, L., L. R. McCloskey, and R. E. Marian. 1981. Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration1. Limnology and Oceanography 26:601-611.
    Nahon, S., N. B. Richoux, J. Kolasinski, M. Desmalades, C. F. Pages, G. Lecellier, S. Planes, and V. B. Lecellier. 2013. Spatial and temporal variations in stable carbon (δ13C) and nitrogen (δ15N) isotopic composition of symbiotic scleractinian corals. PLoS One 8:e81247.
    Newsome, S. D., C. Martinez del Rio, S. Bearhop, and D. L. Phillips. 2007. A niche for isotopic ecology. Frontiers in Ecology and the Environment 5:429-436.
    Obura, D. O. 2009. Reef corals bleach to resist stress. Marine pollution bulletin 58:206-212.
    Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. O’hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, and H. Wagner. 2013. Package ‘vegan’. Community ecology package, version 2:1-295.
    Oliver, T. A., and S. R. Palumbi. 2009. Distributions of stress-resistant coral symbionts match environmental patterns at local but not regional scales. Marine Ecology Progress Series 378:93-103.
    Oliver, T. A., and S. R. Palumbi. 2011a. Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429-440.
    Oliver, T. A., and S. R. Palumbi. 2011b. Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30:241-250.
    Pachauri, R. K., M. R. Allen, V. R. Barros, J. Broome, W. Cramer, R. Christ, J. A. Church, L. Clarke, Q. Dahe, and P. Dasgupta. 2014. Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the fifth assessment report of the Intergovernmental Panel on Climate Change. Ipcc.
    Palardy, J. E., L. J. Rodrigues, and A. G. Grottoli. 2008. The importance of zooplankton to the daily metabolic carbon requirements of healthy and bleached corals at two depths. Journal of Experimental Marine Biology and Ecology 367:180-188.
    Palumbi, S. R., D. J. Barshis, N. Traylor-Knowles, and R. A. Bay. 2014. Mechanisms of reef coral resistance to future climate change. Science 344:895-898.
    Pandolfi, J. M., R. H. Bradbury, E. Sala, T. P. Hughes, K. A. Bjorndal, R. G. Cooke, D. McArdle, L. McClenachan, M. J. H. Newman, G. Paredes, R. R. Warner, and J. B. C. Jackson. 2003. Global Trajectories of the Long-Term Decline of Coral Reef Ecosystems. Science 301:955-958.
    Peir, J.-J. 2011. Power Uprate Effect on Thermal Effluent of Nuclear Power Plants in Taiwan. Page Ch. 13 in P. Tsvetkov, editor. Nuclear Power - Operation, Safety and Environment. InTech, Rijeka.
    Pernice, M., S. R. Dunn, L. Tonk, S. Dove, I. Domart-Coulon, P. Hoppe, A. Schintlmeister, M. Wagner, and A. Meibom. 2015. A nanoscale secondary ion mass spectrometry study of dinoflagellate functional diversity in reef-building corals. Environmental Microbiology 17:3570-3580.
    Pier, J.-J. 2011. Power uprate effect on thermal effluent of nuclear power plants in Taiwan. Page 287 in P. Tsvetkov, editor. Nuclear power - operation, safety and environment. InTech Publication.
    Pigliucci, M., C. J. Murren, and C. D. Schlichting. 2006. Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology 209:2362-2367.
    Plass-Johnson, J. G., V. N. Bednarz, J. M. Hill, J. Jompa, S. C. Ferse, and M. Teichberg. 2018. Contrasting responses in the niches of two coral reef herbivores along a gradient of habitat disturbance in the Spermonde Archipelago, Indonesia. Frontiers in Marine Science 5:32.
    Putnam, H. M., and R. D. Gates. 2015. Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. Journal of Experimental Biology 218:2365-2372.
    R-Core-Team. 2017. R: A Language and Environment for Statistical Computing. Page R Foundation for Statistical Computing, Vienna, Austria.
    Rahav, O., Z. Dubinsky, Y. Achituv, and P. Falkowski. 1989. Ammonium metabolism in the zooxanthellate coral, Stylophora pistillata. Proceedings of the Royal Society of London. B. Biological Sciences 236:325-337.
    Raymundo, L. J., D. Burdick, W. C. Hoot, R. M. Miller, V. Brown, T. Reynolds, J. Gault, J. Idechong, J. Fifer, and A. Williams. 2019. Successive bleaching events cause mass coral mortality in Guam, Micronesia. Coral Reefs 38:677-700.
    Riegl, B. M., S. J. Purkis, A. S. Al-Cibahy, M. A. Abdel-Moati, and O. Hoegh-Guldberg. 2011. Present Limits to Heat-Adaptability in Corals and Population-Level Responses to Climate Extremes. PLoS One 6:e24802.
    Rinkevich, B. 2019. The Active Reef Restoration Toolbox is a Vehicle for Coral Resilience and Adaptation in a Changing World. Journal of Marine Science and Engineering 7:201.
    Risk, M. J., B. E. Lapointe, O. A. Sherwood, and B. J. Bedford. 2009. The use of δ15N in assessing sewage stress on coral reefs. Marine pollution bulletin 58:793-802.
    Roche, R. C., G. J. Williams, and J. R. Turner. 2018. Towards Developing a Mechanistic Understanding of Coral Reef Resilience to Thermal Stress Across Multiple Scales. Current Climate Change Reports 4:51-64.
    Rodrigues, L. J., and A. G. Grottoli. 2007. Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnology and Oceanography 52:1874-1882.
    Rodrigues, L. J., A. G. Grottoli, and T. K. Pease. 2008. Lipid class composition of bleached and recovering Porites compressa Dana, 1846 and Montipora capitata Dana, 1846 corals from Hawaii. Journal of Experimental Marine Biology and Ecology 358:136-143.
    Rowan, R. 2004. Thermal adaptation in reef coral symbionts. Nature 430:742.
    Rowan, R., and N. Knowlton. 1995. Intraspecific diversity and ecological zonation in coral-algal symbiosis. Procceeding of the National Academy of Sciences of the United States of America 92:2850-2853.
    Rowan, R., N. Knowlton, A. Baker, and J. Jara. 1997. Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265-269.
    Safaie, A., N. J. Silbiger, T. R. McClanahan, G. Pawlak, D. J. Barshis, J. L. Hench, J. S. Rogers, G. J. Williams, and K. A. Davis. 2018. High frequency temperature variability reduces the risk of coral bleaching. Nature Communications 9:1671.
    Salih, A., A. Larkum, G. Cox, M. Kühl, and O. Hoegh-Guldberg. 2000. Fluorescent pigments in corals are photoprotective. Nature 408:850-853.
    Sampayo, E. M., T. Ridgway, P. Bongaerts, and O. Hoegh-Guldberg. 2008. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Procceeding of the National Academy of Sciences of the United States of America 105:10444-10449.
    Sawall, Y., A. Al-Sofyani, E. Banguera-Hinestroza, and C. R. Voolstra. 2014. Spatio-temporal analyses of Symbiodinium physiology of the coral Pocillopora verrucosa along large-scale nutrient and temperature gradients in the Red Sea. PLoS One 9:e103179.
    Sawall, Y., A. Al-Sofyani, S. Hohn, E. Banguera-Hinestroza, C. R. Voolstra, and M. Wahl. 2015. Extensive phenotypic plasticity of a Red Sea coral over a strong latitudinal temperature gradient suggests limited acclimatization potential to warming. Sci. Rep. 5.
    Sawall, Y., M. C. Teichberg, J. Seemann, M. Litaay, J. Jompa, and C. Richter. 2011. Nutritional status and metabolism of the coral Stylophora subseriata along a eutrophication gradient in Spermonde Archipelago (Indonesia). Coral Reefs 30:841-853.
    Scheufen, T., R. Iglesias-Prieto, and S. Enríquez. 2017. Changes in the number of symbionts and Symbiodinium cell pigmentation modulate differentially coral light absorption and photosynthetic performance. Frontiers in Marine Science 4:309.
    Seemann, J., R. Carballo-Bolanos, K. Berry, C. González, C. Richter, and R. Leinfelder. 2012. Importance of heterotrophic adaptations of corals to maintain energy reserves. Pages 9-13 in Proceedings of the 12th International Coral Reef Symposium, Cairns, Australia. International Society for Reef Studies.
    Seemann, J., C. T. González, R. Carballo-Bolaños, K. Berry, G. A. Heiss, U. Struck, and R. R. Leinfelder. 2014. Assessing the ecological effects of human impacts on coral reefs in Bocas del Toro, Panama. Environmental monitoring and assessment 186:1747-1763.
    Selig, E. R., K. S. Casey, and J. F. Bruno. 2012. Temperature-driven coral decline: the role of marine protected areas. Global change biology 18:1561-1570.
    Sheppard, C., A. Sheppard, A. Mogg, D. Bayley, A. C. Dempsey, R. Roche, J. Turner, and S. Purkins. 2017. Coral bleaching and mortality in the Chagos Archipelago. Atoll Res Bull 613:1-26.
    Shick, J. M., and W. C. Dunlap. 2002. Mycosporine-Like Amino Acids and Related Gadusols: Biosynthesis, Accumulation, and UV-Protective Functions in Aquatic Organisms. Annual Review of Physiology 64:223-262.
    Sigman, D. M., K. Karsh, and K. Casciotti. 2009. Ocean process tracers: nitrogen isotopes in the ocean.
    Silverstein, R. N., A. M. S. Correa, and A. C. Baker. 2012. Specificity is rarely absolute in coral−algal symbiosis: implications for coral response to climate change. Proceedings of the Royal Society B: Biological Sciences 279:2609-2618.
    Silverstein, R. N., R. Cunning, and A. C. Baker. 2015. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Global change biology 21:236-249.
    Silverstein, R. N., R. Cunning, and A. C. Baker. 2017. Tenacious D: Symbiodinium in clade D remain in reef corals at both high and low temperature extremes despite impairment. Journal of Experimental Biology 220:1192-1196.
    Skirving, W. J., S. F. Heron, B. L. Marsh, G. Liu, J. L. De La Cour, E. F. Geiger, and C. M. Eakin. 2019. The relentless march of mass coral bleaching: a global perspective of changing heat stress. Coral Reefs 38:547-557.
    Smith, L. W., D. Barshis, and C. Birkeland. 2007. Phenotypic plasticity for skeletal growth, density, and calification of Porites lobata in response to habitat type. Coral Reefs 26:559-567.
    Spalding, M. D., and B. E. Brown. 2015. Warm-water coral reefs and climate change. Science 350:769-771.
    Spash, C. L. 2016. This Changes Nothing: The Paris Agreement to Ignore Reality. Globalizations 13:928-933.
    Stat, M., and R. D. Gates. 2011. Clade D Symbiodinium in scleractinian corals: a "nugget" of hope, a selfish opportunist, an ominous sign, or all of the above? Journal of Marine Biology 2011
    Stat, M., W. K. W. Loh, T. C. LaJeunesse, O. Hoegh-Guldberg, and D. A. Carter. 2009. Stability of coral-endosymbiont associations during and after a thermal stress event in the southern Great Barrier Reef. Coral Reefs 28:709-713.
    Susanto, H. A., M. Komoda, M. Yoneda, A. Kano, M. Tokeshi, and H. Koike. 2013. A stable isotope study of the relationship between coral tissues and zooxanthellae in a seasonal tropical environment of East Kalimantan, Indonesia. International Journal of Marine Science 3.
    Tanaka, Y., A. Suzuki, and K. Sakai. 2018. The stoichiometry of coral-dinoflagellate symbiosis: carbon and nitrogen cycles are balanced in the recycling and double translocation system. The ISME Journal 12:860.
    Tchernov, D., M. Y. Gorbunov, C. de Vargas, S. N. Yadav, A. J. Milligan, M. Häggblom, and P. G. Falkowski. 2004. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proceedings of the National Academy of Sciences 101:13521-13535.
    Thomas, L., N. H. Rose, R. A. Bay, E. H. López, M. K. Morikawa, L. Ruiz-Jones, and S. R. Palumbi. 2018. Mechanisms of Thermal Tolerance in Reef-Building Corals across a Fine-Grained Environmental Mosaic: Lessons from Ofu, American Samoa. Frontiers in Marine Science 4.
    Thompson, D. M., and R. van Woesik. 2009. Corals escape bleaching in regions that recently and historically experienced frequent thermal stress.
    Thornhill, D. J., W. K. Fitt, and G. W. Schmidt. 2006a. Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 25:515-519.
    Thornhill, D. J., T. C. Lajeunesse, D. W. Kemp, W. K. Fitt, and G. W. Schmidt. 2006b. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Marine Biology 148:711-722.
    Thornhill, D. J., Y. Xiang, W. K. Fitt, and S. R. Santos. 2009. Reef endemism, host specificity and temporal stability in populations of symbiotic dinoflagellates from two ecologically dominant Caribbean corals. PLoS One 4:e6262.
    Toller, W. W., R. Rowan, and N. Knowlton. 2001. Zooxanthellae of the Montastraea annularis species complex: patterns of distribution of four taxa of Symbiodinium on different reefs and across depths. Biological Bulletin 201:348-359.
    Torda, G., J. M. Donelson, M. Aranda, D. J. Barshis, L. Bay, M. L. Berumen, D. G. Bourne, N. Cantin, S. Foret, and M. Matz. 2017. Rapid adaptive responses to climate change in corals. Nature Climate Change 7:627.
    Tremblay, P., M. Fine, J. Maguer, R. Grover, and C. Ferrier-Pagès. 2013. Photosynthate translocation increases in response to low seawater pH in a coral-dinoflagellate symbiosis. Biogeosciences 10:3997-4007.
    Tremblay, P., R. Grover, J.-F. Maguer, M. Hoogenboom, and C. Ferrier-Pagès. 2014. Carbon translocation from symbiont to host depends on irradiance and food availability in the tropical coral Stylophora pistillata. Coral Reefs 33:1-13.
    Tremblay, P., J. F. Maguer, R. Grover, and C. Ferrier-Pagès. 2015. Trophic dynamics of scleractinian corals: stable isotope evidence. Journal of Experimental Biology 218:1223-1234.
    Ulstrup, K. E., R. Hill, M. J. H. van Oppen, A. W. D. Larkum, and P. J. Ralph. 2008. Seasonal variation in the photo-physiology of homogeneous and heterogeneous Symbiodinium consortia in two scleractinian corals. Marine Ecology Progress Series 361:139-150.
    Ulstrup, K. E., and M. J. H. van Oppen. 2003. Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Molecular ecology 12:3477-3484.
    Valentine, J. F., and K. L. Heck. 2005. Perspective review of the impacts of overfishing on coral reef food web linkages. Coral Reefs 24:209-213.
    Van Hooidonk, R., J. Maynard, J. Tamelander, J. Gove, G. Ahmadia, L. Raymundo, G. Williams, S. F. Heron, and S. Planes. 2016. Local-scale projections of coral reef futures and implications of the Paris Agreement. Scientific reports 6:39666.
    Van Oppen, M. J., R. D. Gates, L. L. Blackall, N. Cantin, L. J. Chakravarti, W. Y. Chan, C. Cormick, A. Crean, K. Damjanovic, and H. Epstein. 2017. Shifting paradigms in restoration of the world's coral reefs. Global change biology 23:3437-3448.
    van Oppen, M. J., J. K. Oliver, H. M. Putnam, and R. D. Gates. 2015. Building coral reef resilience through assisted evolution. Proceedings of the National Academy of Sciences 112:2307-2313.
    van Oppen, M. J. H., B. J. McDonald, B. Willis, and D. J. Miller. 2001. The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation incomplete lineage sorting, or morphological convergence? Molecular biology and evolution 18:1315-1329.
    van Oppen, M. J. H., E. Puill-Stephan, P. Lundgren, G. De’ath, and L. K. Bay. 2014. First-generation fitness consequences of interpopulational hybridisation in a Great Barrier Reef coral and its implications for assisted migration management. Coral Reefs 33:607-611.
    Van Oppen, M. J. H., P. Souter, E. J. Howells, A. Heyward, and R. Berkelmans. 2011. Novel Genetic Diversity Through Somatic Mutations: Fuel for Adaptation of Reef Corals? Diversity 3:405-423.
    Vander Zanden, M. J., and J. B. Rasmussen. 2001. Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46:2061-2066.
    Vargas-Ángel, B., B. Huntington, R. E. Brainard, R. Venegas, T. Oliver, H. Barkley, and A. Cohen. 2019. El Niño-associated catastrophic coral mortality at Jarvis Island, central Equatorial Pacific. Coral Reefs 38:731-741.
    Wall, C. B., M. Kaluhiokalani, B. N. Popp, M. J. Donahue, and R. D. Gates. 2020. Divergent symbiont communities determine the physiology and nutrition of a reef coral across a light-availability gradient. The ISME Journal:1-14.
    Warner, M., G. Chilcoat, F. McFarland, and W. Fitt. 2002. Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastraea. Marine Biology 141:31-38.
    Warner, M. E., T. C. LaJeunesse, J. D. Robison, and R. M. Thur. 2006. The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: potential implications for coral bleaching. Limnology and Oceanography 51:1887-1897.
    Webster, N. S., and T. B. H. Reusch. 2017. Microbial contributions to the persistence of coral reefs. The ISME Journal 11:2167.
    Weis, V. M. 2008. Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. Journal of Experimental Biology 211:3059-3066.
    Wham, D. C., G. Ning, and T. C. LaJeunesse. 2017. Symbiodinium glynnii sp. nov., a species of stress-tolerant symbiotic dinoflagellates from pocilloporid and montiporid corals in the Pacific Ocean. Phycologia 56:396-409.
    Wheeler, B. 2016. Torchiano, M. lmPerm: Permutation tests for linear models. R Packag Version 210.
    Wilkerson, F., D. Kobayashi, and L. Muscatine. 1988. Mitotic index and size of symbiotic algae in Caribbean reef corals. Coral Reefs 7:29-36.
    Wilkinson, C. 2000. Status of coral reefs of the world: 2000. Australian Institute of Marine Science.
    Wong, C. W. M., N. N. Duprey, and D. M. Baker. 2017. New Insights on the Nitrogen Footprint of a Coastal Megalopolis from Coral-Hosted Symbiodinium δ15N. Environmental Science & Technology 51:1981-1987.
    Xu, L., K. Yu, S. Li, G. Liu, S. Tao, Q. Shi, T. Chen, and H. Zhang. 2017. Interseasonal and interspecies diversities of Symbiodinium density and effective photochemical efficiency in five dominant reef coral species from Luhuitou fringing reef, northern South China Sea. Coral Reefs 36:477-487.

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