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Similarities in biomass and energy reserves among coral colonies from contrasting reef environments

  • Pandolfi, J. M., Connolly, S. R., Marshall, D. J. & Cohen, A. L. Projecting coral reef futures under global warming and ocean acidification. Science 333, 418–422 (2011).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Hughes, T. P. et al. Coral reefs in the Anthropocene. Nature 546, 82–90 (2017).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Ellis, J. I. et al. Multiple stressor effects on coral reef ecosystems. Glob. Change Biol. 25, 4131–4146 (2019).

    Article 
    ADS 

    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).

    Article 
    CAS 

    Google Scholar 

  • Hughes, T. P. et al. Global warming impairs stock–recruitment dynamics of corals. Nature 568, 387–390 (2019).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Selkoe, K. A. et al. A map of human impacts to a “pristine” coral reef ecosystem, the Papahānaumokuākea Marine National Monument. Coral Reefs 28, 635–650 (2009).

    Article 
    ADS 

    Google Scholar 

  • Golbuu, Y. et al. Palau’s coral reefs show differential habitat recovery following the 1998-bleaching event. Coral Reefs 26, 319–332 (2007).

    Article 

    Google Scholar 

  • Bruno, J. F. & Selig, E. R. Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS ONE 2, e711 (2007).

    Article 
    ADS 

    Google Scholar 

  • Oliver, T. A. & Palumbi, S. R. Do fluctuating temperature environments elevate coral thermal tolerance?. Coral Reefs 30, 429–440. https://doi.org/10.1007/s00338-011-0721-y (2011).

    Article 
    ADS 

    Google Scholar 

  • van Woesik, R. et al. Climate-change refugia in the sheltered bays of Palau: Analogs of future reefs. Ecol. Evol. 2, 2474–2484 (2012).

    Article 

    Google Scholar 

  • Hoadley, K. D. et al. Host–symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. Sci. Rep. 9, 1–15 (2019).

    Article 
    CAS 

    Google Scholar 

  • Loya, Y. et al. Coral bleaching: The winners and the losers. Ecol. Lett. 4, 122–131 (2001).

    Article 

    Google Scholar 

  • Putnam, H. M. Avenues of reef-building coral acclimatization in response to rapid environmental change. J. Exp. Biol. 224, jeb239319 (2021).

    Article 

    Google Scholar 

  • Ziegler, M., Seneca, F. O., Yum, L. K., Palumbi, S. R. & Voolstra, C. R. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8, 1–8 (2017).

    Article 

    Google Scholar 

  • Grottoli, A. G., Rodrigues, L. J. & Palardy, J. E. Heterotrophic plasticity and resilience in bleached corals. Nature 440, 1186–1189. https://doi.org/10.1038/nature04565 (2006).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Rodrigues, L. J. & Grottoli, A. G. Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol. Oceanogr. 52, 1874–1882 (2007).

    Article 
    ADS 

    Google Scholar 

  • Houlbrèque, F., Tambutté, E. & Ferrier-Pagès, C. Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata. J. Exp. Mar. Biol. Ecol. 296, 145–166 (2003).

    Article 

    Google Scholar 

  • Hoogenboom, M. O., Connolly, S. R. & Anthony, K. R. N. Biotic and abiotic correlates of tissue quality for common scleractinian corals. Mar. Ecol. Prog. Ser. 438, 119–128 (2011).

    Article 
    ADS 

    Google Scholar 

  • Fitt, W. K., McFarland, F. K., Warner, M. E. & Chilcoat, G. C. Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol. Oceanogr. 45, 677–685 (2000).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Aichelman, H. E. et al. Exposure duration modulates the response of Caribbean corals to global change stressors. Limnol. Oceanogr. 66, 3100–3115 (2021).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Schoepf, V. et al. Annual coral bleaching and the long-term recovery capacity of coral. Proc. R. Soc. B. https://doi.org/10.1098/rspb.2015.1887 (2015).

    Article 

    Google Scholar 

  • Lesser, M. P. Using energetic budgets to assess the effects of environmental stress on corals: Are we measuring the right things?. Coral Reefs 32, 25–33 (2013).

    Article 
    ADS 

    Google Scholar 

  • Harland, A. D., Navarro, J. C., Davies, P. S. & Fixter, L. M. Lipids of some Caribbean and Red Sea corals: Total lipid, wax esters, triglycerides and fatty acids. Mar. Biol. 117, 113–117. https://doi.org/10.1007/BF00346432 (1993).

    Article 
    CAS 

    Google Scholar 

  • Yamashiro, H., Oku, H., Higa, H., Chinen, I. & Sakai, K. Composition of lipids, fatty acids and sterols in Okinawan corals. Comp. Biochem. Phys. B. 122, 397–407. https://doi.org/10.1016/S0305-0491(99)00014-0 (1999).

    Article 

    Google Scholar 

  • Gnaiger, E. & Bitterlich, G. Proximate biochemical composition and caloric content calculated from elemental CHN analysis: A stoichiometric concept. Oecologia 62, 289–298 (1984).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Anthony, K. R. N., Connolly, S. R. & Willis, B. L. Comparative analysis of energy allocation to tissue and skeletal growth in corals. Limnol. Oceanogr. 47, 1417–1429 (2002).

    Article 
    ADS 

    Google Scholar 

  • van Woesik, R., Sakai, K., Ganase, A. & Loya, Y. Revisiting the winners and the losers a decade after coral bleaching. Mar. Ecol. Prog. Ser. 434, 67–76 (2011).

    Article 
    ADS 

    Google Scholar 

  • Golbuu, Y., Gouezo, M., Kurihara, H., Rehm, L. & Wolanski, E. Long-term isolation and local adaptation in Palau’s Nikko Bay help corals thrive in acidic waters. Coral Reefs 35, 909–918. https://doi.org/10.1007/s00338-016-1457-5 (2016).

    Article 
    ADS 

    Google Scholar 

  • Barkley, H. C. et al. Changes in coral reef communities across a natural gradient in seawater pH. Sci. Adv. 1, e1500328. https://doi.org/10.1126/sciadv.1500328 (2015).

    Article 
    ADS 

    Google Scholar 

  • Shamberger, K. E. F. et al. Diverse coral communities in naturally acidified waters of a Western Pacific reef. Geophys. Res. Lett. 41, 499–504 (2013).

    Article 
    ADS 

    Google Scholar 

  • Hoadley, K. D. et al. Different functional traits among closely related algal symbionts dictate stress endurance for vital Indo-Pacific reef-building corals. Glob. Change Biol. 27, 5295–5309 (2021).

    Article 
    CAS 

    Google Scholar 

  • Fabricius, K. E., Mieog, J. C., Colin, P. L., Idip, D. & van Oppen, H. M. J. Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Mol. Ecol. 13, 2445–2458 (2004).

    Article 
    CAS 

    Google Scholar 

  • Kemp, D. W. et al. Corals respond to environmental extremes with trophic plasticity (in revision).

  • Enochs, I. C. et al. Effects of light and elevated pCO2 on the growth and photochemical efficiency of Acropora cervicornis. Coral Reefs 33, 477–485 (2014).

    ADS 

    Google Scholar 

  • Folch, J., Lees, M. & Sloane Stanley, G. H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497–509 (1957).

    Article 
    CAS 

    Google Scholar 

  • Conlan, J. A., Jones, P. L., Turchini, G. M., Hall, M. R. & Francis, D. S. Changes in the nutritional composition of captive early-mid stage Panulirus ornatus phyllosoma over ecdysis and larval development. Aquaculture 434, 159–170 (2014).

    Article 
    CAS 

    Google Scholar 

  • Conlan, J. A., Humphrey, C. A., Severati, A. & Francis, D. S. Influence of different feeding regimes on the survival, growth, and biochemical composition of Acropora coral recruits. PLoS ONE 12, e0188568 (2017).

    Article 

    Google Scholar 

  • Nichols, P. D., Mooney, B. D. & Elliott, N. G. Unusually high levels of non-saponifiable lipids in the fishes escolar and rudderfish: Identification by gas and thin-layer chromatography. J. Chromatogr. A 936, 183–191 (2001).

    Article 
    CAS 

    Google Scholar 

  • Parrish, C. C., Bodennec, G. & Gentien, P. Determination of glycoglycerolipids by Chromarod thin-layer chromatography with Iatroscan flame ionization detection. J. Chromatogr. A 741, 91–97 (1996).

    Article 
    CAS 

    Google Scholar 

  • McLachlan, R., Price, H., Dobson, K., Weisleder, N. & Grottoli, A. G. Microplate assay for quantification of soluble protein in ground coral samples. Protocolsio (2020).

  • Masuko, T. et al. Carbohydrate analysis by a phenol–sulfuric acid method in microplate format. Anal. Biochem. 339, 69–72 (2005).

    Article 
    CAS 

    Google Scholar 

  • Anthony, K. R. N., Hoogenboom, M. O., Maynard, J. A., Grottoli, A. G. & Middlebrook, R. Energetics approach to predicting mortality risk from environmental stress: A case study of coral bleaching. Funct. Ecol. 23, 539–550. https://doi.org/10.1111/j.1365-2435.2008.01531.x (2009).

    Article 

    Google Scholar 

  • Rodrigues, L. J., Grottoli, A. G. & Pease, T. K. Lipid class composition of bleached and recovering Porites compressa Dana, 1846 and Montipora capitata Dana, 1846 corals from Hawaii. J. Exp. Mar. Biol. Ecol. 358, 136–143. https://doi.org/10.1016/j.jembe.2008.02.004 (2008).

    Article 
    CAS 

    Google Scholar 

  • Kochman, N.A.-R., Grover, R., Rottier, C., Ferrier-Pages, C. & Fine, M. The reef building coral Stylophora pistillata uses stored carbohydrates to maintain ATP levels under thermal stress. Coral Reefs 40, 1473–1485 (2021).

    Article 

    Google Scholar 

  • Loya, Y. et al. Coral bleaching: The winners and the losers. Eco. Lett. 4, 122–131 (2001).

    Article 

    Google Scholar 

  • Thornhill, D. J. et al. A connection between colony biomass and death in Caribbean reef-building corals. PLoS ONE 6, e29535. https://doi.org/10.1371/journal.pone.0029535 (2011).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Porter, J. W., Fitt, W. K., Spero, H. J., Rogers, C. S. & White, M. W. Bleaching in reef corals: physiological and stable isotopic responses. Proc. Natl. Acad. Sci. USA 86, 9342–9346 (1989).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Brown, B. E. Coral bleaching: Causes and consequences. Coral Reefs 16, S129–S138 (1997).

    Article 

    Google Scholar 

  • Fitt, W. K. et al. Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: The host does matter in determining the tolerance of corals to bleaching. J. Exp. Mar. Biol. Ecol. 373, 102–110. https://doi.org/10.1016/j.jembe.2009.03.011 (2009).

    Article 

    Google Scholar 

  • Stimson, J. S. Location, quantity and rate of change in quantity of lipids in tissue of Hawaiian hermatypic corals. B. Mar. Sci. 41, 889–904 (1987).

    ADS 

    Google Scholar 

  • Grottoli, A. G., Rodrigues, L. J. & Juarez, C. Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar. Biol. https://doi.org/10.1007/s00227-004-1337-3 (2004).

    Article 

    Google Scholar 

  • Yamashiro, H., Oku, H. & Onaga, K. Effect of bleaching on lipid content and composition of Okinawan corals. Fish. Sci. 71, 448–453. https://doi.org/10.1111/j.1444-2906.2005.00983.x (2005).

    Article 
    CAS 

    Google Scholar 

  • Fitt, W. K., Spero, H. J., Halas, J., White, M. W. & Porter, J. W. Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean “bleaching event”. Coral Reefs 12, 57–64 (1993).

    Article 
    ADS 

    Google Scholar 

  • DeSalvo, M. K. et al. Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol. Ecol. 17, 3952–3971. https://doi.org/10.1111/j.1365-294X.2008.03879.x (2008).

    Article 
    CAS 

    Google Scholar 

  • Kenkel, C. D., Meyer, E. & Matz, M. V. Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments. Mol. Ecol. 22, 4322–4334. https://doi.org/10.1111/mec.12390 (2013).

    Article 
    CAS 

    Google Scholar 

  • van Woesik, R. et al. Coral-bleaching responses to climate change across biological scales. Glob. Change Biol. 28, 4229–4250 (2022).

    Article 

    Google Scholar 

  • Brown, B. E., Downs, C. A., Dunne, R. P. & Gibb, S. W. Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Mar. Ecol. Prog. Ser. 242, 119–129 (2002).

    Article 
    ADS 

    Google Scholar 

  • Houlbrèque, F. & Ferrier-Pagès, C. Heterotrophy in tropical scleractinian corals. Biol. Rev. 84, 1–17. https://doi.org/10.1111/j.1469-185X.2008.00058.x (2009).

    Article 

    Google Scholar 

  • Ferrier-Pages, C., Witting, J., Tambutte, E. & Sebens, K. P. Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22, 229–240 (2003).

    Article 

    Google Scholar 

  • Solomon, S. L. et al. Lipid class composition of annually bleached Caribbean corals. Mar. Biol. 167, 1–15 (2020).

    Google Scholar 

  • Matsuya, Z. Some hydrographical studies of the water of Iwayama Bay in the South Seas Islands. Palao Trop. Biol. Stat. St. 1, 95–135 (1937).

    Google Scholar 

  • Tokioka, T. Systematic studies of the plankton organisms occurring in Iwayama Bay, Palao. I. Introductory Notes, with Some References to the Surface Water Temperature and the Settling Volume of Planktons in the Bay. Palao Trop. Biol. Stn Stud. 2, 507–519 (1942).

  • Kurihara, H. et al. Potential local adaptation of corals at acidified and warmed Nikko Bay. Palau. Sci. Rep. 11, 1–10 (2021).

    Google Scholar 

  • Allemand, D., Tambutté, É., Zoccola, D. & Tambutté, S. Coral Calcification, Cells to Reefs (Springer, 2011).

    Book 

    Google Scholar 

  • Pan, T. C. F., Applebaum, S. L. & Manahan, D. T. Experimental ocean acidification alters the allocation of metabolic energy. Proc. Nat. Acad. Sci.-Biol. 112, 4696–4701 (2015).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • Wall, C. B., Mason, R. A. B., Ellis, W. R., Cunning, R. & Gates, R. D. Elevated pCO2 affects tissue biomass composition, but not calcification, in a reef coral under two light regimes. R. Soc. Open Sci. 4, 170683. https://doi.org/10.1098/rsos.170683 (2017).

    Article 
    CAS 

    Google Scholar 

  • Drenkard, E. J. et al. Juveniles of the Atlantic coral, Favia fragum (Esper, 1797) do not invest energy to maintain calcification under ocean acidification. J. Exp. Mar. Biol. Ecol. 507, 61–69 (2018).

    Article 
    CAS 

    Google Scholar 

  • Parkinson, J. E., Banaszak, A. T., Altman, N. S., LaJeunesse, T. C. & Baums, I. B. Intraspecific diversity among partners drives functional variation in coral symbioses. Sci. Rep. 5, 1–12 (2015).

    Article 

    Google Scholar 

  • Barshis, D. J. et al. Genomic basis for coral resilience to climate change. Proc. Natl. Acad. Sci.-Biol. 110, 1387–1392. https://doi.org/10.1073/pnas.1210224110 (2013).

    Article 
    ADS 

    Google Scholar 

  • Bhattacharya, D. et al. Comparative genomics explains the evolutionary success of reef-forming corals. Elife 5, e13288 (2016).

    Article 

    Google Scholar 

  • Rivera, H. E. et al. Palau’s warmest reefs harbor thermally tolerant corals that thrive across different habitats. Commun. Biol. 5, 1–12 (2022).

    Article 

    Google Scholar 

  • Thomas, L. et al. Mechanisms of thermal tolerance in reef-building corals across a fine-grained environmental mosaic: lessons from Ofu, American Samoa. Front. Mar. Sci. https://doi.org/10.3389/fmars.2017.00434 (2018).

    Article 

    Google Scholar 

  • Manzello, D. P. et al. Role of host genetics and heat-tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming. Glob. Change Biol. 25, 1016–1031. https://doi.org/10.1111/gcb.14545 (2019).

    Article 
    ADS 

    Google Scholar 

  • Dixon, G. B. et al. Genomic determinants of coral heat tolerance across latitudes. Science 348, 1460–1462 (2015).

    Article 
    ADS 
    CAS 

    Google Scholar 

  • van Oppen, M. J. H., Oliver, J. K., Putnam, H. M. & Gates, R. D. Building coral reef resilience through assisted evolution. Proc. Natl. Acad. Sci. USA 112, 2307–2313 (2015).

    Article 
    ADS 

    Google Scholar 

  • Suggett, D. J., Warner, M. E. & Leggat, W. Symbiotic dinoflagellate functional diversity mediates coral survival under ecological crisis. Trends Ecol. Evol. 32, 735–745. https://doi.org/10.1016/j.tree.2017.07.013 (2017).

    Article 

    Google Scholar 

  • Nitschke, M. R. et al. The Diversity and Ecology of Symbiodiniaceae: A Traits-Based Review. (Academic Press, 2022).

  • Battista, T. A., Costa, B. M. & Anderson, S. M. Shallow-Water Benthic Habitats of the Republic of Palau. (US Department of Commerce, National Oceanic and Atmospheric Administration, 2007).

  • Anderson, M. NCCOS Benthic Habitats of Palau Derived From IKONOS Imagery, 2003–2006. (2007).


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