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). More