Mass extinctions and ocean acidification: biological constraints on geological dilemmas

Abstract

The five mass extinction events that the earth has so far experienced have impacted coral reefs as much or more than any other major ecosystem. Each has left the Earth without living reefs for at least four million years, intervals so great that they are commonly referred to as ‘reef gaps’ (geological intervals where there are no remnants of what might have been living reefs). The causes attributed to each mass extinction are reviewed and summarised. When these causes and the reef gaps that follow them are examined in the light of the biology of extant corals and their Pleistocene history, most can be discarded. Causes are divided into (1) those which are independent of the carbon cycle: direct physical destruction from bolides, ‘nuclear winters’ induced by dust clouds, sea-level changes, loss of area during sea-level regressions, loss of biodiversity, low and high temperatures, salinity, diseases and toxins and extraterrestrial events and (2) those linked to the carbon cycle: acid rain, hydrogen sulphide, oxygen and anoxia, methane, carbon dioxide, changes in ocean chemistry and pH. By process of elimination, primary causes of mass extinctions are linked in various ways to the carbon cycle in general and ocean chemistry in particular with clear association with atmospheric carbon dioxide levels. The prospect of ocean acidification is potentially the most serious of all predicted outcomes of anthropogenic carbon dioxide increase. This study concludes that acidification has the potential to trigger a sixth mass extinction event and to do so independently of anthropogenic extinctions that are currently taking place.

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References

  1. Alvarez L, Alvarez W, Asaro F, Michel HV (1980) Extraterrestrial cause for the Cretaceous-Tertiary extinction: experimental results and theoretical interpretation. Science 208:1095–1108

    PubMed  Article  CAS  Google Scholar 

  2. Archer D (2005) Fate of fossil fuel CO2 in geological time. J Geophys Res 111:C09S05. doi:10.1029/2004JC002625

    Article  CAS  Google Scholar 

  3. Barron EJ (1983) A warm, equable Cretaceous: the nature of the problem. Earth Sci Rev 19:305–338

    Article  Google Scholar 

  4. Barron EJ, Washington WM (1985) Warm cretaceous climates: high atmospheric CO2 as a plausible mechanism. In: Sundquist ET, Broecker WS (eds) The carbon cycle and atmospheric CO2: natural variations, Archaean to Present. Geophys Monogr 32:546–553

  5. Beauvais L (1984) Evolution and diversification of Jurassic Scleractinia. Palaeontogr Am 54:219–224

    Google Scholar 

  6. Berner RA (1993) Weathering and its effect on atmospheric CO2 over Phanerozoic time. Chem Geol 107:373–374

    Article  Google Scholar 

  7. Berner RA (1994) GEOCARB II: a revised model of atmospheric CO2 over Phanerozoic time. Am J Sci 294:56–91

    CAS  Google Scholar 

  8. Berner RA (2006) Inclusion of the weathering of volcanic rocks in the GEOCARBSULF model. Am J Sci 306:295–302

    Article  CAS  Google Scholar 

  9. Briggs JC (1991) A Cretaceous-Tertiary mass extinction? Bioscience 41:619–624

    PubMed  Article  CAS  Google Scholar 

  10. Buddemeier RW, Kleypas JA, Aronson RB (2004) Coral reefs and global climate change: potential contributions of climate change to stresses on coral reef ecosystems. Pew Center on Global Climate Change, Arlington

    Google Scholar 

  11. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365

    PubMed  Article  CAS  Google Scholar 

  12. Copper P (1994) Ancient reef ecosystem expansion and collapse. Coral Reefs 13:3–11

    Article  Google Scholar 

  13. Copper P (2001) Evolution, radiations, and extinctions in Proterozoic to Mid-Paleozoic reefs. In: Stanley GD Jr (ed) The history and sedimentology of ancient reef systems. Academic/Plenum Publishers, New York, pp 89–119

    Google Scholar 

  14. Copper P (2002) Silurian and Devonian reefs: 80 million years of global greenhouse between two ice ages. In: Kiessling W, Flügel E, Galonka J (eds) Phanerozoic Reef Patterns. SEPM (Soc Sediment Geol) Spec Publ 72:181–238

  15. Erwin DH (2006) Extinction: how life on earth nearly ended 250 million years ago. Princeton University Press, Princeton

    Google Scholar 

  16. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas JV, Fabry J, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366

    PubMed  Article  CAS  Google Scholar 

  17. Fine M, Tchernov D (2007) Scleractinian coral species survive and recover from decalcification. Science 315:1811

    PubMed  Article  CAS  Google Scholar 

  18. Flügel E, Senowbari-Daryan B (2001) Triassic reefs of the Tethys. In: Stanley GD Jr (ed) The history and sedimentology of ancient reef systems. Academic/Plenum Publishers, New York, pp 217–249

    Google Scholar 

  19. Gale A (2000) The Cretaceous world. In: Culver SJ, Rawson PF (eds) Biotic response to global change: the last 145 million years. Cambridge University Press, Cambridge, pp 4–19

    Google Scholar 

  20. Gattuso J-P, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am Zool 39:160–183

    CAS  Google Scholar 

  21. Glen W (1990) What killed the dinosaurs? Am Sci 78:354–370

    Google Scholar 

  22. Guinotte JM, Buddemeier RW, Kleypas JA (2003) Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22:551–558

    Article  Google Scholar 

  23. Hallam A, Wignall PB (1997) Mass extinctions and their aftermath. Oxford University Press, Oxford

    Google Scholar 

  24. Hautmann M (2004) Effect of End-Triassic CO2 maximum on carbonate sedimentation and marine mass extinction. Facies 50:257–261

    Article  Google Scholar 

  25. IPCC (2007) Summary for Policymakers. In: Solomon S, Quin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University press, Cambridge, pp 1–18

    Google Scholar 

  26. Jablonski D (1986) Mass extinctions: new answers, new questions. In: Kaufman L, Mallory K (eds) The last extinction. MIT Press, Cambridge, pp 43–61

    Google Scholar 

  27. Johnson CC, Sanders D, Kauffman EG, Hay WW (2002) Patterns and processes influencing Upper Cretaceous reefs. In: Kiessling W, Flügel E, Galonka J (eds) Phanerozoic reef patterns. SEPM (Soc Sediment Geol) Spec Publ 72:549–585

  28. Keller G, Adatte T, Stinnesbeck W, Stüben D, Berner Z, Kramer U, Harting M (2004) More evidence that the Chicxulub impact predates the K/T mass extinction. Meteoritics Planet Sci 39:1127–1144

    CAS  Article  Google Scholar 

  29. Kiessling W (2001) Phanerozoic reef trends based on the Paleoreef database. In: Stanley GD Jr (ed) The history and sedimentology of ancient reef systems. Academic/Plenum Publishers, New York, pp 41–88

    Google Scholar 

  30. Kleypas JA, Langdon C (2006) Coral reefs and changing seawater carbonate chemistry. In: Phinney JT, Hoegh-Guldberg O, Kleypas JA, Skirving W, Strong A (eds) Coral reefs and climate change: science and management. Coast Estuar Stud 61:73–110

  31. Kleypas JA, Danabasoglu G, Lough JM (2008) Potential role of the ocean thermostat in determining regional differences in coral reef bleaching events. Geophys Res Lett 35:L03613. doi:10.1029/2007GL032257

    Article  Google Scholar 

  32. Knoll AH, Bambach RK, Payne JL, Pruss S, Fischer WW (2007) Paleophysiology and end-Permian mass extinction. Earth Planet Sci Lett 256:295–313

    Article  CAS  Google Scholar 

  33. Lambeck K, Chappell J (2001) Sea level change through the last glacial cycle. Science 292:679–686

    PubMed  Article  CAS  Google Scholar 

  34. MacLeod N, Rawson N, Forey PF, Banner FT, Boudagher-Fadel MK, Brown PR, Burnett JA, Chambers P, Culver S, Evans SE, Jeffery C, Kaminski MA, Lord AR, Milner AC, Milner AR, Morris N, Owen E, Rosen BR, Smith AB, Taylor PD, Urquhart E, Young JR (1997) The Cretaceous-Tertiary biotic transition. Journal of the Geological Society, London 154:265–292

    Article  Google Scholar 

  35. Marubini F, Ferrier-Pages C, Cuif J-P (2002) Suppression of skeletal growth in scleractinian corals by decreasing ambient carbonate-ion concentration: a cross-family comparison. Proc R Soc Lond B Biol Sci 270:179–184

    Article  Google Scholar 

  36. McLaren DJ, Goodfellow WD (1990) Geological and biological consequences of giant impacts. Annu Rev Earth Planet Sci 18:123–171

    Article  Google Scholar 

  37. Raup DM, Sepkoski JJ Jr (1986) Periodic extinction of families and genera. Science 231:833–836

    PubMed  Article  CAS  Google Scholar 

  38. Raven J, Caldeira K, Elderfield H, Hoegh-Guldberg O, Liss P, Riebesell U, Shepherd J, Turley C, Watson A (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Policy Document 12/05, Royal Society, London

  39. Riebesell U, Zondervan I, Rost B, Tortell PD, Zeebe RE, Morel FMM (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407:364–367

    PubMed  Article  CAS  Google Scholar 

  40. Ries JB, Stanley SM, Hardie LA (2006) Scleractinian corals produce calcite, and grow more slowly, in artificial Cretaceous seawater. Geology 34:525–528

    Article  Google Scholar 

  41. Rosen BR (2000) Algal symbiosis and the collapse and recovery of reef communities: Lazarus corals across the Cretaceous/Tertiary boundary. In: Culver SJ, Rawson PF (eds) Biotic response to global change: the last 145 million years. Cambridge University Press, Cambridge, pp 164–180

    Google Scholar 

  42. Rosen BR, Turnšek D (1989) Extinction patterns and biogeography of scleractinian corals across the Cretaceous/Tertiary boundary. Memoir of the Association of Australasian Palaeontologists 8:355–370

    Google Scholar 

  43. Rosenberg E, Ben-Haim Y (2002) Microbial diseases in corals and global warming. Environ Microbiol 4:318–326

    PubMed  Article  Google Scholar 

  44. Rothschild LJ, Lister AM (eds) (2003) Evolution on planet earth: the impact of the physical environment. Academic Press, London

    Google Scholar 

  45. Ryskin G (2003) Methane-driven oceanic eruptions and mass extinctions. Geology 31:741–744

    Article  CAS  Google Scholar 

  46. Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng T-H, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371

    PubMed  Article  CAS  Google Scholar 

  47. Selig ER, Drew Harvell C, Bruno JF, Willis BL, Page CA, Casey KS, Sweatman H (2006) Analysis and relationship between ocean temperature anomalies and coral disease outbreaks at broad spatial scales. In: Phinney JT, Hoegh-Guldberg O, Kleypas J, Skirving W, Strong A (eds) Coral reefs and climate change: science and management. Coast Estuar Stud 61:111–128

  48. Sepkowski JJ Jr (1995) Patterns of Phanerozoic extinction: a perspective from global databases. In: Walliser OH (ed) Global events and event stratigraphy. Springer-Verlag, Berlin, pp 35–51

    Google Scholar 

  49. Sepkowski JJ Jr (2002) A compendium of fossil marine animal genera. Bull Am Paleontol 363:1–563

    Google Scholar 

  50. Siddall M, Siddall EJ, Rohling A, Almogi-Labin C, Hemleben D, Meischner I, Schmelzer I, Smeed DA (2003) Sea-level fluctuations during the last glacial cycle. Nature 423:853–858

    PubMed  Article  CAS  Google Scholar 

  51. Stanley GD Jr (1988) The history of early Mesozoic reef communities: a three-step process. Palaios 3:170–183

    Article  Google Scholar 

  52. Stanley GD Jr (2001) Introduction to reef ecosystems and their evolution. In: Stanley GD Jr (ed) The history and sedimentology of ancient reef systems. Academic/Plenum Publishers, New York, pp 1–39

    Google Scholar 

  53. Stanley SM, Hardie LA (1998) Secular oscillations in the carbonate mineralogy of reef-building and sediment-producing organisms driven by tectonically forced shifts in seawater chemistry. Palaeogeogr Palaeoclimatol Palaeoecol 144:3–19

    Article  Google Scholar 

  54. Stolarski J, Meibom A, Przenioslo R, Mazur M (2007) A Cretaceous scleractinian coral with a calcitic skeleton. Science 318:92–94

    PubMed  Article  CAS  Google Scholar 

  55. Tajika E (1999) Carbon cycle and climate change during the Cretaceous inferred from a biogeochemical carbon cycle model. The Island Arc 8:293–303

    Article  CAS  Google Scholar 

  56. Toon OB, Zahnle K, Morrison D, Turco RP, Covey C (1997) Environmental perturbations caused by the impacts of asteroids and comets. Rev Geophys 35:41–78

    Article  CAS  Google Scholar 

  57. Turley CM, Roberts JM, Guinotte JM (2007) Corals in deep-water: will the unseen hand of ocean acidification destroy cold-water ecosystems? Coral Reefs 26:445–448

    Article  Google Scholar 

  58. Veron JEN (1995) Corals in space and time: the biogeography and evolution of the Scleractinia. University of New South Wales Press, Sydney

    Google Scholar 

  59. Veron JEN (2008) A reef in time: the Great Barrier Reef from beginning to end. Harvard University Press, Cambridge

    Google Scholar 

  60. Veron JEN, Kelly R (1988) Species stability in hermatypic corals of Papua New Guinea and the Indo-Pacific. Memoir of the Association of Australasian Palaeontologists 6:1–69

    Google Scholar 

  61. Webby BD (1992) Global biogeography of Ordovician corals and stromatoporoids. In: Webby B, Laurie JR (eds) Global perspectives on Ordovician geology 2. Balkema, Rotterdam, pp 261–276

  62. Wood R (1999) Reef evolution. Oxford University Press, Oxford

    Google Scholar 

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Acknowledgements

I thank Katharina Fabricius for inviting me to write this article and three anonymous reviewers for their efforts.

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Correspondence to J. E. N. Veron.

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Communicated by Guest Editor Dr. Katharina Fabricius.

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Veron, J.E.N. Mass extinctions and ocean acidification: biological constraints on geological dilemmas. Coral Reefs 27, 459–472 (2008). https://doi.org/10.1007/s00338-008-0381-8

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Keywords

  • Ocean acidification
  • Mass extinctions
  • Climate change
  • Coral reefs
  • Corals