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Heat stress differentially impacts key calcification mechanisms in reef-building corals

Abstract

Coral reefs are increasingly threatened by climate change, mass bleaching events and ocean acidification (OA). Coral calcification, a process that is critical to build and maintain the structure of tropical coral reefs, is highly sensitive to both warming and acidifying oceans. However, in contrast to the impacts of OA on coral calcification, significant knowledge gaps remain regarding how coral biomineralization mechanisms are impacted by heat stress and bleaching. Using a combined physiological and geochemical approach, we investigated how a marine heatwave impacted coral symbiotic status (chlorophyll a, algal symbiont density), the carbonate chemistry of the coral calcifying fluid (via δ11B and B/Ca) and skeletal trace element composition in the branching coral Acropora aspera. Importantly, we recorded in situ temperature throughout the bleaching event and recovery as well as coral symbiotic status during peak bleaching and after 7 months of recovery. We show that heat-stressed Acropora corals continued to upregulate the pH of their calcifying fluid (cf); however, dissolved inorganic carbon upregulation inside the cf was significantly disrupted by heat stress. Similarly, we observed suppression of the typical seasonality in the trace element (TE) temperature proxies Sr/Ca, Mg/Ca, Li/Ca and Li/Mg, indicating disruption of important calcification mechanisms, Rayleigh fractionation and reduced growth rates. Anomalies in TE/Ca ratios were still observed 7 months after peak bleaching, even though algal symbiont densities and chlorophyll a concentrations were fully restored at this point. Interestingly, the biomineralization response to heat stress did not differ between thermally distinct reef habitats harbouring coral populations with different heat tolerance, nor between heat-stressed colonies with different severity of bleaching. Our findings suggest that coral biomineralization mechanisms in Acropora are highly sensitive to heat stress, showing similar patterns of biogeochemical stress response as other coral taxa.

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Data availability

The data that support the findings of this study are available from the corresponding author, [VS], upon reasonable request.

References

  • Akiva A, Neder M, Kahil K, Gavriel R, Pinkas I, Goobes G, Mass T (2018) Minerals in the pre-settled coral Stylophora pistillata crystallize via protein and ion changes. Nat Commun 9:1880

    PubMed  PubMed Central  Google Scholar 

  • Al-Horani FA, Al-Moghrabi SM, de Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426

    CAS  Google Scholar 

  • Allison N, Cohen I, Finch AA, Erez J (2011) Controls on Sr/Ca and Mg/Ca in scleractinian corals: the effects of Ca-ATPase and transcellular Ca channels on skeletal chemistry. Geochim Cosmochim Acta 75:6350–6360

    CAS  Google Scholar 

  • Barott KL, Perez SO, Linsmayer LB, Tresguerres M (2015) Differential localization of ion transporters suggests distinct cellular mechanisms for calcification and photosynthesis between two coral species. Am J Physiol Integr Comp Physiol 309:R235–R246

    CAS  Google Scholar 

  • Bernardet C, Tambutté E, Techer N, Tambutté S, Venn AA (2019) Ion transporter gene expression is linked to the thermal sensitivity of calcification in the reef coral Stylophora pistillata. Sci Rep 9:18676

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cai W-J, Ma Y, Hopkinson BM, Grottoli AG, Warner ME, Ding Q, Hu X, Yuan X, Schoepf V, Xu H, Han C, Melman TF, Hoadley KD, Pettay DT, Matsui Y, Baumann JH, Levas S, Ying Y, Wang Y (2016) Microelectrode characterization of coral daytime interior pH and carbonate chemistry. Nat Commun 7:11144

    CAS  PubMed  PubMed Central  Google Scholar 

  • Camp EF, Schoepf V, Mumby PJ, Hardtke LA, Rodolfo-Metalpa R, Smith DJ, Suggett DJ (2018) The future of coral reefs subject to rapid climate change: lessons from natural extreme environments. Front Mar Sci 5:4. https://doi.org/10.3389/fmars.2018.00004

    Article  Google Scholar 

  • Carilli JE, Norris RD, Black BA, Walsh SM, McField M (2009) Local stressors reduce coral resilience to bleaching. Publ Libr Sci One 4:e6324. https://doi.org/10.1371/journal.pone.0006324

    CAS  Article  Google Scholar 

  • Chan NCS, Connolly SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob Chang Biol 19:282–290

    PubMed  Google Scholar 

  • Clarke H, D’Olivo JP, Conde M, Evans RD, McCulloch MT (2019) Coral records of variable stress impacts and possible acclimatization to recent marine heat wave events on the northwest shelf of Australia. Paleoceanogr Paleoclimatology 34:1672–1688

    Google Scholar 

  • Clarke H, D’Olivo JP, Falter J, Zinke J, Lowe R, McCulloch M (2017) Differential response of corals to regional mass-warming events as evident from skeletal Sr/Ca and Mg/Ca ratios. Geochemistry, Geophys Geosystems n/a-n/a

    Google Scholar 

  • Cohen AL, McConnaughey TA (2003) Geochemical perspectives on coral mineralization. Rev Mineral Geochemistry 54:151–187

    CAS  Google Scholar 

  • Cornwall CE, Comeau S, DeCarlo TM, Moore B, D’Alexis Q, McCulloch MT (2018) Resistance of corals and coralline algae to ocean acidification: physiological control of calcification under natural pH variability. Proc R Soc B Biol Sci 285:20181168. https://doi.org/10.1098/rspb.2018.1168

    CAS  Article  Google Scholar 

  • D’Olivo JP, Ellwood G, DeCarlo TM, McCulloch MT (2019a) Deconvolving the long-term impacts of ocean acidification and warming on coral biomineralisation. Earth Planet Sci Lett 526:115785

    Google Scholar 

  • D’Olivo JP, Georgiou L, Falter J, DeCarlo TM, Irigoien X, Voolstra CR, Roder C, Trotter J, McCulloch MT (2019b) Long-term impacts of the 1997–1998 bleaching event on the growth and resilience of massive Porites corals from the central Red Sea. Geochemistry, Geophys Geosystems

    Google Scholar 

  • D’Olivo JP, McCulloch MT (2017) Response of coral calcification and calcifying fluid composition to thermally induced bleaching stress. Sci Rep 7:2207

    PubMed  PubMed Central  Google Scholar 

  • D’Olivo JP, McCulloch MT, Judd K (2013) Long-term records of coral calcification across the central great barrier reef: assessing the impacts of river runoff and climate change. Coral Reefs 32:999–1012

    Google Scholar 

  • Dandan SS, Falter JL, Lowe RJ, McCulloch MT (2015) Resilience of coral calcification to extreme temperature variations in the Kimberley region, northwest Australia. Coral Reefs 34:1151–1163

    Google Scholar 

  • DeCarlo TM (2018) Characterizing coral skeleton mineralogy with Raman spectroscopy. Nat Commun 9:5325

    PubMed  PubMed Central  Google Scholar 

  • DeCarlo TM, Comeau S, Cornwall CE, McCulloch MT (2018) Coral resistance to ocean acidification linked to increased calcium at the site of calcification. Proc R Soc B Biol Sci 285

  • Dishon G, Fisch J, Horn I, Kaczmarek K, Bijma J, Gruber DF, Nir O, Popovich Y, Tchernov D (2015) A novel paleo-bleaching proxy using boron isotopes and high-resolution laser ablation to reconstruct coral bleaching events. Biogeosciences pp 5677–5687

  • Drake JL, Mass T, Stolarski J, Von Euw S, van de Schootbrugge B, Falkowski PG (2020) How corals made rocks through the ages. Glob Chang Biol 26:31–53

    PubMed  Google Scholar 

  • Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, Alvarez-Filip L, Baca B, Bartels E, Bastidas C, Bouchon C, Brandt M, Bruckner AW, Bunkley-Williams L, Cameron A, Causey BD, Chiappone M, Christensen TRL, Crabbe MJC, Day O, de la Guardia E, Diaz-Pulido G, DiResta D, Gil-Agudelo DL, Gilliam DS, Ginsburg RN, Gore S, Guzman HM, Hendee JC, Hernandez-Delgado EA, Husain E, Jeffrey CFG, Jones RJ, Jordan-Dahlgren E, Kaufman LS, Kline DI, Kramer PA, Lang JC, Lirman D, Mallela J, Manfrino C, Marechal J-P, Marks K, Mihaly J, Miller WJ, Mueller EM, Muller EM, Orozco Toro CA, Oxenford HA, Ponce-Taylor D, Quinn N, Ritchie KB, Rodriguez S, Ramirez AR, Romano S, Samhouri JF, Sanchez JA, Schmahl GP, Shank BV, Skirving WJ, Steiner SCC, Villamizar E, Walsh SM, Walter C, Weil E, Williams EH, Roberson KW, Yusuf Y (2010) Caribbean corals in crisis: Record thermal stress, bleaching, and mortality in 2005. Publ Libr Sci One 5:e13969

    Google Scholar 

  • Von Euw S, Zhang Q, Manichev V, Murali N, Gross J, Feldman LC, Gustafsson T, Flach C, Mendelsohn R, Falkowski PG (2017) Biological control of aragonite formation in stony corals. Science 356(80):933–938

    Google Scholar 

  • Gaetani GA, Cohen AL (2006) Element partitioning during precipitation of aragonite from seawater: a framework for understanding paleoproxies. Geochim Cosmochim Acta 70:4617–4634

    CAS  Google Scholar 

  • Gilmour JP, Cook KL, Ryan NM, Puotinen ML, Green RH, Shedrawi G, Hobbs JPA, Thomson DP, Babcock RC, Buckee J, Foster T, Richards ZT, Wilson SK, Barnes PB, Coutts TB, Radford BT, Piggott CH, Depczynski M, Evans SN, Schoepf V, Evans RD, Halford AR, Nutt CD, Bancroft KP, Heyward AJ, Oades D (2019) The state of Western Australia’s coral reefs. Coral Reefs 38:651–667

    Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    CAS  PubMed  Google Scholar 

  • Holcomb M, DeCarlo TM, Gaetani GA, McCulloch M (2016) Factors affecting B/Ca ratios in synthetic aragonite. Chem Geol 437:67–76

    CAS  Google Scholar 

  • Holcomb M, Tambutté E, Allemand D, Tambutté S (2014) Light enhanced calcification in Stylophora pistillata: effects of glucose, glycerol and oxygen. PeerJ 2:e375

    PubMed  PubMed Central  Google Scholar 

  • Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge T, Claar DC, Eakin CAM, Gilmour JP, Graham NAJ, Harrison H, Hobbs JPA, Hoey AS, Hoogenboom MO, Lowe RJ, McCulloch M, Pandolfi JM, Pratchett MS, Schoepf V, Torda G, Wilson SK (2018) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83

    CAS  PubMed  Google Scholar 

  • Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs JPA, Hoogenboom MO, Kennedy EV, Kuo CY, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377

    CAS  Google Scholar 

  • Kornder NA, Riegl BM, Figueiredo J (2018) Thresholds and drivers of coral calcification responses to climate change. Glob Chang Biol 24:5084–5095

    PubMed  Google Scholar 

  • Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, Van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131

    Google Scholar 

  • Marshall JF, McCulloch MT (2002) An assessment of the Sr/Ca ratio in shallow water hermatypic corals as a proxy for sea surface temperature. Geochim Cosmochim Acta 66:3263–3280

    CAS  Google Scholar 

  • Mass T, Drake JL, Haramaty L, Kim JD, Zelzion E, Bhattacharya D, Falkowski PG (2013) Cloning and characterization of four novel coral acid-rich proteins that precipitate carbonates in vitro. Curr Biol 23:1126–1131

  • Mass T, Giuffre AJ, Sun CY, Stifler CA, Frazier MJ, Neder M, Tamura N, Stan CV, Marcus MA, Gilbert PUPA (2017) Amorphous calcium carbonate particles form coral skeletons. Proc Natl Acad Sci U S A 114:E7670–E7678

    CAS  PubMed  PubMed Central  Google Scholar 

  • McCulloch MT, D’Olivo JP, Falter J, Holcomb M, Trotter JA (2017) Coral calcification in a changing World and the interactive dynamics of pH and DIC upregulation. Nat Commun 8:15686

    CAS  PubMed  PubMed Central  Google Scholar 

  • McCulloch MT, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2:623–627

    CAS  Google Scholar 

  • McCulloch MT, Holcomb M, Rankenburg K, Trotter J (2014) Rapid, high-precision measurements of boron isotopic compositions in marine carbonates. Rapid Commun Mass Spectrom 28:1–9

    Google Scholar 

  • Montagna P, McCulloch M, Douville E, Correa ML, Trotter J, Rodolfo-Metalpa R, Dissard D, Ferrier-Pages C, Frank N, Freiwald A (2014) Li/Mg systematics in scleractinian corals: Calibration of the thermometer. Geochim Cosmochim Acta 132:288–310

    CAS  Google Scholar 

  • Le Nohaïc M, Ross CL, Cornwall CE, Comeau S, Lowe R, McCulloch MT, Schoepf V (2017) Marine heatwave causes unprecedented regional mass bleaching of thermally resistant corals in northwestern Australia. Sci Rep 7:14999. https://doi.org/10.1038/s41598-017-14794-y

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–898

    CAS  PubMed  Google Scholar 

  • von Reumont J, Hetzinger S, Garbe-Schönberg D, Manfrino C, Dullo W-C (2016) Impact of warming events on reef-scale temperature variability as captured in two Little Cayman coral Sr/Ca records. Geochem Geophys Geosyst 17:846–857

    Google Scholar 

  • Reynaud S, Ferrier-Pagès C, Meibom A, Mostefaoui S, Mortlock R, Fairbanks R, Allemand D (2007) Light and temperature effects on Sr/Ca and Mg/Ca ratios in the scleractinian coral Acropora sp. Geochim Cosmochim Acta 71:354–362

    CAS  Google Scholar 

  • Riegl B, Purkis SJ, Al-Cibahy AS, Al-Harthi S, Grandcourt E, Al-Sulaiti K, Baldwin J, Abdel-Moati MA (2012) Coral bleaching and mortality thresholds in the SE Gulf: Highest in the world. In: Riegl B, Purkis SJ (eds) Coral reefs of the gulf: adaptation to climatic extremes. Springer, Berlin, pp 95–105

    Google Scholar 

  • Ries JB (2011) A physicochemical framework for interpreting the biological calcification response to CO2-induced ocean acidification. Geochim Cosmochim Acta 75:4053–4064

    CAS  Google Scholar 

  • Rocker MM, Noonan S, Humphrey C, Moya A, Willis BL, Bay LK (2015) Expression of calcification and metabolism-related genes in response to elevated pCO2 and temperature in the reef-building coral Acropora millepora. Mar Genomics 24:313–318

    PubMed  Google Scholar 

  • Rollion-Bard C, Blamart D (2015) Possible controls on Li, Na, and Mg incorporation into aragonite coral skeletons. Chem Geol 396:98–111

    CAS  Google Scholar 

  • Ross CL, DeCarlo TM, McCulloch MT (2018) Environmental and physiochemical controls on coral calcification along a latitudinal temperature gradient in Western Australia. Glob Chang Biol 25(2):431–447

    PubMed  Google Scholar 

  • Ross CL, DeCarlo TM, McCulloch MT (2019) Calibration of Sr/Ca. Li/Mg and Sr-U paleothermometry in branching and foliose corals, Paleoceanogr Paleoclimatology

    Google Scholar 

  • Schoepf V, Carrion SA, Pfeifer SM, Naugle M, Dugal L, Bruyn J, McCulloch M (2019) Stress-resistant corals may not acclimatize to ocean warming but maintain heat tolerance under cooler temperatures. Nat Commun 10:4031

    PubMed  PubMed Central  Google Scholar 

  • Schoepf V, Jung MU, McCulloch MT, White N, Stat M, Thomas L (2020) Thermally variable, macrotidal reef habitats promote rapid recovery from mass coral bleaching. Front Mar Sci 7:245

    Google Scholar 

  • Schoepf V, Jury CP, Toonen RJ, McCulloch MT (2017) Coral calcification mechanisms facilitate adaptive responses to ocean acidification. Proc R Soc B Biol Sci 284:20172117

    Google Scholar 

  • Schoepf V, McCulloch MT, Warner ME, Levas SJ, Matsui Y, Aschaffenburg M, Grottoli AG (2014) Short-term coral bleaching is not recorded by skeletal boron isotopes. Publ Libr Sci One 9:e112011

    Google Scholar 

  • Schoepf V, Stat M, Falter JL, McCulloch MT (2015) Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment. Sci Rep 5:17639

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sevilgen DS, Venn AA, Hu MY, Tambutté E, De Beer D, Planas-Bielsa V, Tambutté S (2019) Full in vivo characterization of carbonate chemistry at the site of calcification in corals. Sci Adv 5(1):eaau7447

    PubMed  PubMed Central  Google Scholar 

  • Siebeck UE, Marshall NJ, Klüter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460

    Google Scholar 

  • Sinclair DJ (2005) Correlated trace element “vital effects” in tropical corals: a new geochemical tool for probing biomineralization. Geochim Cosmochim Acta 69:3265–3284

    CAS  Google Scholar 

  • Sun C-Y, Stifler CA, Chopdekar R V., Schmidt CA, Parida G, Schoeppler V, Fordyce BI, Brau JH, Mass T, Tambutté S, Gilbert PUPA (2020) From particle attachment to space-filling coral skeletons. Proc Natl Acad Sci pp 2020–2025

  • Trotter J, Montagna P, McCulloch MT, Silenzi S, Reynaud S, Mortimer G, Martin S, Ferrier-Pages C, Gattuso J-P, Rodolfo-Metalpa R (2011) Quantifying the pH “vital effect” in the temperate zooxanthellate coral Cladocora caespitosa: Validation of the boron seawater pH proxy. Earth Planet Sci Lett 303:163–173

    CAS  Google Scholar 

  • Venn AA, Bernardet C, Chabenat A, Tambutté E, Tambutté S (2020) Paracellular transport to the coral calcifying medium: effects of environmental parameters. J Exp Biol 223:17

    Google Scholar 

  • Venn AA, Tambutte E, Holcomb M, Laurent J, Allemand D, Tambutte S (2013) Impact of seawater acidification on pH at the tissue-skeleton interface and calcification in reef corals. Proc Natl Acad Sci 110:1634–1639

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank: J. Brown, G. Firman and the staff at Cygnet Bay Pearl Farm for assistance in the field; the Bardi Jawi people who enabled this research through their advice and consent to access their traditional lands; S. Comeau and C. Cornwall for sharing carbonate chemistry data; C. Ross for sharing unpublished Li/Ca data; K. Rankenburg, H. Sanderson and E. Larcombe for assistance in the lab. Funding was provided by the PADI Foundation (VS, Research Grant #21737), Australian Research Council Centre of Excellence for Coral Reef Studies (MM, CE140100020) and an ARC Laureate Fellowship (MM, LF120100049).

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VS, JPD and MM designed the study. VS conducted the fieldwork and statistical analyses. CR and MJ conducted the physiological analyses. VS and JPD conducted the geochemical analyses. VS led the writing of the paper, with all authors contributing to the final manuscript.

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Correspondence to Verena Schoepf.

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Schoepf, V., D’Olivo, J., Rigal, C. et al. Heat stress differentially impacts key calcification mechanisms in reef-building corals. Coral Reefs 40, 459–471 (2021). https://doi.org/10.1007/s00338-020-02038-x

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Keywords

  • Calcification mechanisms
  • Heat stress
  • Coral bleaching
  • Calcifying fluid
  • Boron isotopes
  • Trace elements