Abstract
Changes in the atmospheric partial pressure of CO2 (pCO2) leads to predictable impacts on the surface ocean carbonate system. Here, the importance of atmospheric pCO2 <260 ppmv is established for the optimum performance (and stability) of the algal endosymbiosis employed by a key suite of tropical reef-building coral species. Violation of this symbiotic threshold is revealed as a prerequisite for major historical reef extinction events, glacial–interglacial feedback climate cycles, and the modern decline of coral reef ecosystems. Indeed, it is concluded that this symbiotic threshold enacts a fundamental feedback mechanism needed to explain the characteristic dynamics (and drivers) of the coupled land–ocean–atmosphere carbon cycle of the Earth System since the mid-Miocene, some 25 million yr ago.
Similar content being viewed by others
References
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
Alley RB, Mayewski PA, Sowers M, Stuiver M, Taylor KC, Clark PU (1997) Holocene climatic instability: a prominent, widespread event 8200 yr ago. Geology 25:483–486
Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci U S A 105:17442–17446
Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23:539–550
Archer D, Winguth A, Lea D, Mahowald N (2000) What caused the glacial/interglacial atmospheric pCO2 cycles? Rev Geophys 38:159–189
Ashkenazy Y, Gildor H (2008) Timing and significance of maximum and minimum equatorial insolation. Paleoceanography 23:PA1206
Barber RT, Chavez FP (1991) Regulation of primary productivity rate in the Equatorial Pacific. Limnol Oceanogr 36:1803–1815
Bard E, Hamelin B, Delanghe-Sabatier D (2010) Deglacial meltwater pulse 1B and the Younger Dryas sea levels revisited with boreholes at Tahiti. Science 327:1235–1237
Bell PRF (1992) Eutrophication and coral reefs—some examples in the Great Barrier Reef Lagoon. Water Res 26:553–568
Berger A, Loutre MF, Mélice JL (2006) Equatorial insolation: from precession harmonics to eccentricity frequencies. Climate of the Past 2:131–136
Berger WH (1982) Increase of carbon dioxide in the atmosphere during deglaciation: the coral reef hypothesis. Naturwissenschaften 69:87–88
Broecker WS, Peng TH (1987) The role of CaCO3 compensation in the glacial to interglacial CO2 change. Paleoceanography 13:352–364
Broecker WS, Henderson G (1998) The sequence of events surrounding termination II and their implications for the cause of glacial–interglacial CO2 changes. Paleoceanogr 4:352–364
Broecker WS, Lao Y, Klas M, Clark E, Bonami G, Ivy S, Chen C (1993) A search for an early Holocene CaCO3 preservation event. Paleoceanography 8:333–339
Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327
Budd AF (2000) Diversity and extinction in the Cenozoic history of Caribbean reefs. Coral Reefs 19:25–35
Budd AF, Johnson KG (1999) Origination preceding extinction during late Cenozoic turnover of Caribbean reefs. Paleobiology 25:188–200
Cabioch G, Banks-Cutler KA, Beck WJ, Burr GS, Corrège T, Lawrence Edwards R, Taylor FW (2003) Continuous reef growth during the last 23 cal kyr BP in a tectonically active zone (Vanuatu, south-west Pacific). Quat Sci Rev 22:1771–1786
Calvo E, Pelejero C, Pena LD, Cacho I, Logan GA (2011) Eastern Equatorial Pacific productivity and related CO2 changes since the last glacial period. Proc Natl Acad Sci U S A 108:5537–5541
Chauvin A, Denis V, Cuet P (2011) Is the response of coral calcification to seawater acidification related to nutrient loading? Coral Reefs 30:911–923
Crawley A, Kline DI, Dunn S, Anthony K, Dove S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Glob Chang Biol 16:851–863
Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat Clim Chang 3:259–262
Denny MW (1988) Biology and the mechanics of the wave-swept environment. Princeton University Press, Princeton, NJ, p 329
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 12:5677–5687
Drew EA (1972) The biology and physiology of alga–invertebrate symbiosis II. The density of symbiotic algal cells in a number of hermatypic hard corals and alcyonarians from various depths. J Exp Mar Bio Ecol 9:71–75
Edinger EN, Risk MJ (1995) Oligocene-Miocene extinction and geographic restriction of Caribbean corals: roles of turbidity, temperature, and nutrients. Palaios 9:576–598
Fairbanks RG (1989) A 17,000-year glacio-eustatic sea level record: influence of glacial melting rates on the Younger Dryas event and deep-ocean circulation. Nature 342:637–642
Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. Bioscience 43:606–611
Fine M, Gildor H, Genin A (2013) A coral reef refuge in the Red Sea. Glob Chang Biol 19:3640–3647
Flores JA, Marino M, Sierro FJ, Hodell DA, Charles CD (2003) Calcareous plankton dissolution pattern and coccolithophore assemblages during the last 600 kyr at ODP Site 1089 (Cape Basin, South Atlantic): paleoceanographic implications. Paleogeogr Paleoclim Paleoecol 196:409–426
Frankignoulle M, Canon C, Gattuso JP (1994) Marine calcification as a source of carbon dioxide: Positive feedback of increasing atmospheric CO2. Limnol Oceanogr 39:458–462
Gleason DF, Wellington GM (1993) Ultraviolet radiation and coral bleaching. Nature 365:836–838
Glynn PW (1990) Coral mortality and disturbance to coral reefs in the tropical Eastern Pacific. In: Glynn PW (ed) Global ecological consequences of the 1982–83 El Niño-Southern Oscillation. Elsevier, Amsterdam, pp 55–126
Gordillo FJL, Jiménez C, Figueroa FL, Niell FX (2003) Influence of elevated CO2 and nitrogen supply on the carbon assimilation performance and cell composition of the unicellular alga Dunaliella viridis. Physiol Plant 119:513–518
Grover R, Maguer J-F, Reynaud-Vaganay S, Ferrier-Pagès C (2002) Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammonium concentrations. Limnol Oceanogr 47:782–790
Hallock P, Schlager W (1986) Nutrient excess and the demise of coral reefs and carbonate platforms. Palaios 1:389–398
Hodell DA, Charles CD, Sierro FJ (2001) Late Pleistocene evolution of the ocean’s carbonate system. Earth Planet Sci Lett 192:109–124
Hoegh-Guldberg O, Muscatine L, Goiran C, Siggaard D, Marion G (2004) Nutrient-induced perturbations to & #x03B4;13C and & #x03B4;15 N in symbiotic dinoflagellates and their hosts. Mar Ecol Prog Ser 280:105–114
Hoogenboom M, Beraud E, Ferrier-Pageś C (2010) Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa. Coral Reefs 29:21–29
Hubbard DK (2009) Depth-related and species-related patterns of Holocene reef accretion in the Caribbean and western Atlantic: a critical assessment of existing models. Inn: Swart PK, Eberli GP, McKenzie JA (eds) Perspectives in carbonate geology: a tribute to the career of Robert Nathan Ginsburg. Special publication 41 of the IAS. Wiley & Sons, Hoboken, NJ, pp 1–18
Hughen KA, Overpeck JT, Peterson LC, Trumbore S (1996) Rapid climate changes in the tropical Atlantic region during the last deglaciation. Nature 380:51–54
Johnson KG, Budd AF, Stemann TA (1995) Extinction selectivity and ecology of Neogene Caribbean corals. Paleobiology 21:52–73
Kaniewska P, Chan C-KK, Kline D, Ling EYS, Rosic N, Edwards D, Hoegh-Guldberg O, Dove S (2015) Transcriptomic changes in coral holobionts provide insights into physiological challenges of future climate and ocean change. PLoS One 10:e0139223
Kawahata H, Suzuki A, Goto K (1997) Coral reef ecosystems as a source of atmospheric CO2: evidence from pCO2 measurements of surface waters. Coral Reefs 16:261–266
Kienast M, Kienast SS, Calvert SE, Eglinton TI, Mollenhauer G, Francois R, Mix AC (2006) Eastern Pacific cooling and Atlantic overturning circulation during the last deglaciation. Nature 443:846–849
Kiessling W, Simpson C, Beck B, Mewis H, Pandolfi JM (2012) Equatorial decline of reef corals during the last Pleistocene interglacial. Proc Natl Acad Sci U S A 109:21378–21383
Klöcker R, Henrich R (2006) Recent and Late Quaternary pteropod preservation on the Pakistan shelf and continental slope. Mar Geol 231:103–111
Krief S, Hendy EJ, Fine M, Yam R, Meibom A, Foster GL, Shemesh A (2010) Physiological and isotopic responses of scleractinian corals to ocean acidification. Geochim Cosmochim Acta 74:4988–5001
Kubota K, Yokoyama Y, Ishikawa T, Obrochta S, Suzuki A (2014) Larger CO2 source at the equatorial Pacific during the last deglaciation. Sci Rep 4:5261
Lapointe BE, Littler MM, Littler DS (1993) Modification of benthic community structure by natural eutrophication. Proc 7th Int Coral Reef Symp 1:323–334
Lesser M, Stat M, Gates RD (2013) The endosymbiotic dinoflagellates (Symbiodinium sp.) of coral are parasites and mutualists. Coral Reefs 32:603–611
Lovelock JE, Margulis LM (1974) Atmospheric homeostasis by and for the biosphere: the Gaia hypothesis. Tellus 26:2–10
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
Marchitto TM, Lynch-Stieglitz J, Hemming SR (2005) Deep Pacific CaCO3 compensation and glacial–interglacial atmospheric CO2. Earth Planet Sci Lett 231:317–336
Mewis H (2016) Ecological stability of Indo-Pacific coral reefs during Quaternary climatic fluctuations. PhD Thesis, Humboldt University, Berlin, Germany
Monnin E, Indermühle A, Dällenbach A, Flückiger J, Stauffer B, Stocker TF, Raynaud D, Barnola J-M (2001) Atmospheric CO2 concentrations over the last glacial termination. Science 291:112–114
Montaggioni LF (2000) Postglacial reef growth. C R Acad Sci II 331:319–330
Montaggioni LF (2005) History of Indo-Pacific coral reef systems since the last glaciation: development patterns and controlling factors. Earth Sci Rev 71:1–75
Muscatine L, Ferrier-Pages C, Blackburn A, Gates RD, Baghdasarian G, Allemand D (1998) Cell-specific density of symbiotic dinoflagellates in tropical anthozoans. Coral Reefs 17:329–337
Naim O (1993) Seasonal responses of a fringing reef community to eutrophication (Réunion Island, western Indian Ocean). Mar Ecol Prog Ser 99:137–151
Najjar RG (1992) Marine biogeochemistry. In: Trenberth K (ed) Climate system. Cambridge University Press, Cambridge, UK, pp 241–280
Nir O, Gruber DF, Shemesh E, Glasser E, Tchernov D (2014) Seasonal mesophotic coral bleaching of Stylophora pistillata in the northern Red Sea. PLoS One 9:e84968
Pearson PN, Palmer MR (2000) Atmospheric carbon dioxide concentrations over the past 60 million years. Nature 406:695–699
Perry CT, Edinger EN, Kench PS, Murphy GN, Smithers SG, Steneck RS, Mumby PJ (2012) Estimating rates of biologically driven coral reef framework production and erosion: a new census-based carbonate budget methodology and applications to the reefs of Bonaire. Coral Reefs 31:853–868
Renema W, Pandolfi JM, Kiessling W, Bosellini FR, Klaus JS, Korpanty C, Rosen B, Santodomingo N, Wallace CC, Webster JM, Johnson KG (2016) Are coral reefs victims of their own past success? Sci Adv 2:e1500850
Reynaud S, Leclercq N, Romaine-Lioud S, Ferrier-Pagés C, Jaubert J, Gattuso J-P (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob Chang Biol 9:1660–1668
Ridgwell AJ, Watson AJ, Maslin MA, Kaplan JO (2003) Implications of coral buildup for the controls on atmospheric CO2 since the Last Glacial Maximum. Paleoceanography 18:1083
Sheppard CRC (2003) Predicted recurrences of mass mortality in the Indian Ocean. Nature 435:294–297
Sigenthaler U, Stocker TF, Monnin E, Lüthi D, Schwander J, Stauffer B, Raynaud D, Barnola J-M, Fischer H, Masson-Delmotte V, Jouzel J (2005) Stable carbon cycle-climate relationship during the late Pleistocene. Science 310:1313–1317
Sigman DM, Boyle EA (2000) Glacial–interglacial variations in atmospheric carbon dioxide. Nature 407:859–869
Stanford JD, Hemingway R, Rohling EJ, Challenor PG, Medina-Elizalde M, Lester AJ (2010) Sea-level probability for the last deglaciation: a statistical analysis of far-field records. Glob Planet Change 79:193–203
Stanley GD (2006) Photosymbiosis and the evolution of modern coral reefs. Science 312:857–858
Starzak DE, Quinnell RG, Nitschke MR, Davy SK (2014) The influence of symbiont type on photosynthetic carbon flux in a model cnidarian–dinoflagellate symbiosis. Mar Biol 161:711–724
Vecsei A, Berger WH (2004) Increase of atmospheric CO2 during deglaciation: constraints on the coral reef hypothesis from patterns of deposition. Global Biogeochem Cycles 18:GB1035
Wolf-Gladrow DA, Riebesell U, Burkhardt S, Bijma J (1999) Direct effects of CO2 concentrations on growth and isotopic composition of marine plankton. Tellus B Chem Phys Meteorol 51:461–476
Wooldridge SA (2009) A new conceptual model for the warm-water breakdown of the coral–algae endosymbiosis. Mar Freshw Res 60:483–496
Wooldridge SA (2010) Is the coral–algae symbiosis really mutually beneficial for the partners? BioEssays 32:615–625
Wooldridge SA (2012) A hypothesis linking sub-optimal seawater pCO2 conditions for cnidarian–Symbiodinium symbioses with the exceedence of the interglacial threshold (> 260 ppmv). Biogeosciences 9:1709–1723
Wooldridge SA (2013) Breakdown of the coral–algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae. Biogeosciences 10:1647–1658
Wooldridge SA (2014a) Differential thermal bleaching susceptibilities amongst coral taxa: reposing the role of the host. Coral Reefs 33:15–27
Wooldridge SA (2014b) Formalising a mechanistic linkage between heterotrophic feeding and thermal bleaching resistance. Coral Reefs 33:1131–1136
Wooldridge SA (2016) Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reef locations: 1. Identifying threshold of concern for the Great Barrier Reef, Australia. Mar Pollut Bull. doi:10.1016/j.marpolbul.2016.04.054
Wooldridge SA, Brodie JA, Furnas M (2006) Exposure of inner shelf reefs to nutrient enriched runoff entering the Great Barrier Reef Lagoon: post-European changes and the design of water quality targets. Mar Pollut Bull 52:1467–1479
Wooldridge SA, Brodie JE, Kroon FJ, Turner RDR (2015) Ecologically based targets for bioavailable (reactive) nitrogen discharge from the drainage basins of the Wet Tropics region, Great Barrier Reef. Mar Pollut Bull 97:262–272
Wooldridge SA, Done T, Berkelmans R, Jones R, Marshall P (2005) Precursors for resilience in coral communities in a warming climate: a belief network approach. Mar Ecol Prog Ser 295:157–169
Wooldridge SA, Done TJ, Thomas CR, Gordon I, Marshall PA, Jones R (2012) Safeguarding coastal coral communities on the central Great Barrier Reef against climate change: realizable local and global actions. Clim Change 112:945–961
Wooldridge SA, Heron SF, Brodie JE, Done TJ, Masiri I, Hinrichs S (2017) Excess seawater nutrients, enlarged algal symbiont densities and bleaching sensitive reef locations: 2. A regional-scale predictive model for the Great Barrier Reef, Australia. Mar Pollut Bull 114:343–354
Yellowlees D, Rees TA, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694
Yentsch CS, Yentsch CM, Cullen JJ, Lapointe B, Phinney DA, Yentsch SW (2002) Sunlight and water transparency: cornerstones in coral research. J Exp Mar Bio Ecol 268:171–183
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Anastazia Banaszak
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wooldridge, S.A. Instability and breakdown of the coral–algae symbiosis upon exceedence of the interglacial pCO2 threshold (>260 ppmv): the “missing” Earth-System feedback mechanism. Coral Reefs 36, 1025–1037 (2017). https://doi.org/10.1007/s00338-017-1594-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-017-1594-5