Current Climate Change Reports

, Volume 3, Issue 4, pp 271–281 | Cite as

The Role of Natural Variability in Shaping the Response of Coral Reef Organisms to Climate Change

  • Emily B. Rivest
  • Steeve Comeau
  • Christopher E. Cornwall
Corals and Climate Change (C Langdon, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Corals and Climate Change


Purpose of Review

We investigate whether regimes of greater daily variability in temperature or pH result in greater tolerance to ocean warming and acidification in key reef-building taxa (corals, coralline algae).

Recent Findings

Temperature and pH histories will likely influence responses to future warming and acidification. Past exposure of corals to increased temperature variability generally leads to greater thermotolerance. However, the effects of past pH variability are unclear. Variability in pH or temperature will likely modify responses during exposure to stressors, independent of environmental history. In the laboratory, pH variability often limited the effects of ocean acidification, but the effects of temperature variability on responses to warming were equivocal.


Environmental variability could alter responses of coral reef organisms to climate change. Determining how both environmental history as well as the direct impacts of environmental variability will interact with the effects of anthropogenic climate change should now be high priority.


Environmental variability Ocean acidification Ocean warming Coral Crustose coralline algae Calcification 



We thank Emma Camp for sharing the raw data from her study. We also acknowledge Kristy Kroeker and Sarah Lummis for their contributions in designing and assembling a database of studies that test the effects of changes in carbonate chemistry on corals. This paper is Contribution No. 3677 of the Virginia Institute of Marine Science, College of William & Mary.


Funding was provided to SC by an ARC Discovery Early Career Researcher Award (DE160100668).

Compliance with Ethical Standards

Conflict of Interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

40641_2017_82_MOESM1_ESM.docx (15.1 mb)
ESM 1 (DOCX 15447 kb)


  1. 1.
    Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, et al. Coral reefs under rapid climate change and ocean acidification. Science. 2007;318:1737–42.CrossRefGoogle Scholar
  2. 2.
    Hughes TP, Kerry JT, Álvarez-Noriega M, et al. Global warming and recurrent mass bleaching of corals. Nature. 2017;543:373–7.CrossRefGoogle Scholar
  3. 3.
    Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Robbins LL (2006) Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research. Report of a workshop held 18–20 April 2005, St. Petersburg, FL, sponsored by NSF, NOAA, and the US Geological Survey, 88 pp.Google Scholar
  4. 4.
    Pörtner H-O, Farrell AP. Physiology and climate change. Science. 2008;322:690–2.CrossRefGoogle Scholar
  5. 5.
    van Oppen MJH, Oliver JK, Putnam HM, Gates RD. Building coral reef resilience through assisted evolution. Proc Natl Acad Sci U S A. 2015;112:2307–13.CrossRefGoogle Scholar
  6. 6.
    Boyd PW, Cornwall CE, Davison A, Doney SC, Fourquez M, Hurd CL, et al. Biological responses to environmental heterogeneity under future ocean conditions. Glob Chang Biol. 2016;22:2633–50.CrossRefGoogle Scholar
  7. 7.
    Reusch TBH, Boyd PW. Experimental evolution meets marine phytoplankton. Evolution. 2013;67:1849–59.CrossRefGoogle Scholar
  8. 8.
    Hoegh-Guldberg O. Climate change and coral reefs: Trojan horse or false prophecy? Coral Reefs. 2009;28:569–75.CrossRefGoogle Scholar
  9. 9.
    Falter JL, Lowe RJ, Zhang Z, McCulloch M, Douillet P. Physical and biological controls on the carbonate chemistry of coral reef waters: effects of metabolism, wave forcing, sea level, and geomorphology. PLoS One. 2013;8:e53303.CrossRefGoogle Scholar
  10. 10.
    Lee H-J, Chao S-Y, Fan K-L, Kuo T-Y. Tide-induced eddies and upwelling in a semi-enclosed basin: Nan Wan. Estuar Coast Shelf Sci. 1999;49:775–87.CrossRefGoogle Scholar
  11. 11.
    Mongin M, Baird ME, Tilbrook B, Matear RJ, Lenton A, Herzfeld M, et al. The exposure of the Great Barrier Reef to ocean acidification. Nat Commun. 2016;7:10732.CrossRefGoogle Scholar
  12. 12.
    Kleypas JA, Anthony KRN, Gattuso J-P. Coral reefs modify their seawater carbon chemistry—case study from a barrier reef (Moorea, French Polynesia). Glob Chang Biol. 2011;17:3667–78.CrossRefGoogle Scholar
  13. 13.
    Page HN, Andersson AJ, Jokiel PL, Rodgers KS, Lebrato M, Yeakel K, et al. Differential modification of seawater carbonate chemistry by major coral reef benthic communities. Coral Reefs. 2016;35:1311–25.CrossRefGoogle Scholar
  14. 14.
    Delille B, Delille D, Fiala M, Prevost C, Frankignoulle M. Seasonal changes of pCO2 over a subantarctic Macrocystis kelp bed. Polar Biol. 2000;23:706–16.CrossRefGoogle Scholar
  15. 15.
    Andersson AJ, Gledhill D. Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Annu Rev Mar Sci. 2013;5:321–48.CrossRefGoogle Scholar
  16. 16.
    Andersson AJ, Yeakel KL, Bates NR, de Putron SJ. Partial offsets in ocean acidification from changing coral reef biogeochemistry. Nat Clim Chang. 2013;4:56–61.CrossRefGoogle Scholar
  17. 17.
    Anthony KRN, Diaz-Pulido G, Verlinden N, Tilbrook B, Andersson AJ. Benthic buffers and boosters of ocean acidification on coral reefs. Biogeosciences. 2013;10:4897–909.CrossRefGoogle Scholar
  18. 18.
    Woods JD, Barkmann W. The response of the upper ocean to solar heating. I: the mixed layer. Q J R Meteorol Soc. 1986;112:1–27.CrossRefGoogle Scholar
  19. 19.
    Falter JL, Zhang Z, Lowe RJ, McGregor F, Keesing J, McCulloch MT. Assessing the drivers of spatial variation in thermal forcing across a nearshore reef system and implications for coral bleaching. Limnol Oceanogr. 2014;59:1241–55.CrossRefGoogle Scholar
  20. 20.
    Ohde S, van Woesik R. Carbon dioxide flux and metabolic processes of a coral reef, Okinawa. Bull Mar Sci. 1999;65:559–76.Google Scholar
  21. 21.
    Santos IR, Glud RN, Maher D, Erler D, Eyre BD. Diel coral reef acidification driven by porewater advection in permeable carbonate sands, Heron Island, Great Barrier Reef. Geophys Res Lett. 2011;38:L03604.CrossRefGoogle Scholar
  22. 22.
    Gruber RK, Lowe RJ, Falter JL. Metabolism of a tide-dominated reef platform subject to extreme diel temperature and oxygen variations. Limnol Oceanogr. 2017;62:1701–17.CrossRefGoogle Scholar
  23. 23.
    Comeau S, Edmunds P, Spindel N, Carpenter R. Diel pCO2 oscillations modulate the response of the coral Acropora hyacinthus to ocean acidification. Mar Ecol Prog Ser. 2014;501:99–111.CrossRefGoogle Scholar
  24. 24.
    Koweek D, Dunbar RB, Rogers JS, Williams GJ, Price N, Mucciarone D, et al. Environmental and ecological controls of coral community metabolism on Palmyra Atoll. Coral Reefs. 2015;34:339–51.CrossRefGoogle Scholar
  25. 25.
    Padilla-Gamiño JL, Gaitán-Espitia JD, Kelly MW, Hofmann GE. Physiological plasticity and local adaptation to elevated pCO2 in calcareous algae: an ontogenetic and geographic approach. Evol Appl. 2016;9:1043–53.CrossRefGoogle Scholar
  26. 26.
    Vargas CA, Lagos NA, Lardies MA, Duarte C, Manriquez PH, Aguilera VM, et al. Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity. Nat Ecol Evol. 2017;1:84.CrossRefGoogle Scholar
  27. 27.
    West-Eberhard M. Developmental plasticity and evolution. New York: Oxford University Press; 2003.Google Scholar
  28. 28.
    Schaum CE, Collins S. Plasticity predicts evolution in a marine alga. Proc R Soc Lond B Biol Sci. 2014;281:20141486.CrossRefGoogle Scholar
  29. 29.
    Kenkel CD, Almanza AT, Matz MV. Fine-scale environmental specialization of reef-building corals might be limiting reef recovery in the Florida Keys. Ecology. 2015;96:3197–212.CrossRefGoogle Scholar
  30. 30.
    Boyd PW, Dillingham PW, McGraw CM, Armstrong EA, Cornwall CE, Feng Y-Y, et al. Physiological responses of a Southern Ocean diatom to complex future ocean conditions. Nat Clim Chang. 2015;6:207.Google Scholar
  31. 31.
    Darling ES, McClanahan TR, Côté IM. Life histories predict coral community disassembly under multiple stressors. Glob Chang Biol. 2013;19:1930–40.CrossRefGoogle Scholar
  32. 32.
    Anthony KRN, Kleypas JA, Gattuso J-P. Coral reefs modify their seawater carbon chemistry—implications for impacts of ocean acidification. Glob Chang Biol. 2011;17:3655–66.CrossRefGoogle Scholar
  33. 33.
    Manzello DP, Enochs IC, Melo N, Gledhill DK, Johns EM. Ocean acidification refugia of the Florida reef tract. PLoS One. 2012;7:e41715.CrossRefGoogle Scholar
  34. 34.
    Shaw EC, Munday PL, McNeil BI. The role of CO2 variability and exposure time for biological impacts of ocean acidification. Geophys Res Lett. 2013;40:4685–8.CrossRefGoogle Scholar
  35. 35.
    Yates KK, Rogers CS, Herlan JJ, Brooks GR, Smiley NA, Larson RA. Diverse coral communities in mangrove habitats suggest a novel refuge from climate change. Biogeosciences. 2014;11:4321–37.CrossRefGoogle Scholar
  36. 36.
    Pasparakis C, Davis BE, Todgham AE. Role of sequential low-tide-period conditions on the thermal physiology of summer and winter laboratory-acclimated fingered limpets, Lottia digitalis. Mar Biol. 2016;163:23.CrossRefGoogle Scholar
  37. 37.
    Hettinger A, Sanford E, Hill TM, Russell AD, Sato KNS, Hoey J, et al. Persistent carry-over effects of planktonic exposure to ocean acidification in the Olympia oyster. Ecology. 2012;93:2758–68.CrossRefGoogle Scholar
  38. 38.
    Hettinger A, Sanford E, Hill TM, Lenz EA, Russell AD, Gaylord B. Larval carry-over effects from ocean acidification persist in the natural environment. Glob Chang Biol. 2013;19:3317–26.Google Scholar
  39. 39.
    Nice H, Morritt D, Crane M, Thorndyke M. Long-term and transgenerational effects of nonylphenol exposure at a key stage in the development of Crassostrea gigas. Possible endocrine disruption? Mar Ecol Prog Ser. 2003;256:293–300.CrossRefGoogle Scholar
  40. 40.
    Parker LM, Ross PM, O’Connor WA, Borysko L, Raftos DA, Pörtner H-O. Adult exposure influences offspring response to ocean acidification in oysters. Glob Chang Biol. 2012;18:82–92.CrossRefGoogle Scholar
  41. 41.
    Parker LM, O’Connor WA, Raftos DA, Pörtner H-O, Ross PM. Persistence of positive carryover effects in the oyster, Saccostrea glomerata, following transgenerational exposure to ocean acidification. PLoS One. 2015;10:e0132276.CrossRefGoogle Scholar
  42. 42.
    Uthicke S, Soars N, Foo S, Byrne M. Effects of elevated pCO2 and the effect of parent acclimation on development in the tropical Pacific sea urchin Echinometra mathaei. Mar Biol. 2013;160:1913–26.CrossRefGoogle Scholar
  43. 43.
    Dupont S, Dorey N, Stumpp M, Melzner F, Thorndyke M. Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar Biol. 2013;160:1835–43.CrossRefGoogle Scholar
  44. 44.
    Miller GM, Watson S-A, Donelson JM, McCormick MI, Munday PL. Parental environment mediates impacts of increased carbon dioxide on a coral reef fish. Nat Clim Chang. 2012;2:858–61.CrossRefGoogle Scholar
  45. 45.
    Schade FM, Clemmesen C, Mathias Wegner K. Within- and transgenerational effects of ocean acidification on life history of marine three-spined stickleback (Gasterosteus aculeatus). Mar Biol. 2014;161:1667–76.CrossRefGoogle Scholar
  46. 46.
    Donelson JM, Munday PL, McCormick MI, Pitcher CR. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat Clim Chang. 2011;2:30–2.CrossRefGoogle Scholar
  47. 47.
    Thor P, Dupont S. Transgenerational effects alleviate severe fecundity loss during ocean acidification in a ubiquitous planktonic copepod. Glob Chang Biol. 2015;21:2261–71.CrossRefGoogle Scholar
  48. 48.
    Putnam HM, Gates RD. Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J Exp Biol. 2015;218:2365–72.CrossRefGoogle Scholar
  49. 49.
    Ward S. Evidence for broadcast spawning as well as brooding in the scleractinian coral Pocillopora damicornis. Mar Biol. 1992;112:641–6.CrossRefGoogle Scholar
  50. 50.
    Suckling CC, Clark MS, Beveridge C, Brunner L, Hughes AD, Harper EM, et al. Experimental influence of pH on the early life-stages of sea urchins II: increasing parental exposure times gives rise to different responses. Invertebr Reprod Dev. 2014;58:161–75.CrossRefGoogle Scholar
  51. 51.
    Vandegehuchte MB, Janssen CR. Epigenetics in an ecotoxicological context. Mutat Res Toxicol Environ Mutagen. 2014;764:36–45.CrossRefGoogle Scholar
  52. 52.
    Sanford E, Kelly MW. Local adaptation in marine invertebrates. Annu Rev Mar Sci. 2011;3:509–35.CrossRefGoogle Scholar
  53. 53.
    Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA. Mechanisms of reef coral resistance to future climate change. Science. 2014;344:895–8.CrossRefGoogle Scholar
  54. 54.
    Howells EJ, Beltran VH, Larsen NW, Bay LK, Willis BL, van Oppen MJH. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat Clim Chang. 2012;2:116–20.CrossRefGoogle Scholar
  55. 55.
    Kelly LW, Williams GJ, Barott KL, et al. Local genomic adaptation of coral reef-associated microbiomes to gradients of natural variability and anthropogenic stressors. Proc Natl Acad Sci U S A. 2014;111:10227–32.CrossRefGoogle Scholar
  56. 56.
    Oliver TA, Palumbi SR. Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs. 2011;30:429–40.CrossRefGoogle Scholar
  57. 57.
    Schoepf V, Stat M, Falter JL, McCulloch MT. Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment. Sci Rep. 2015;5:17639.CrossRefGoogle Scholar
  58. 58.
    Rivest EB, Gouhier TC. Complex environmental forcing across the biogeographical range of coral populations. PLoS One. 2015;10:e0121742.CrossRefGoogle Scholar
  59. 59.
    Rivest EB, Chen C-S, Fan T-Y, Li H-H, Hofmann GE. Lipid consumption in coral larvae differs among sites: a consideration of environmental history in a global ocean change scenario. Proc R Soc Lond B Biol Sci. 2017;284:20162825.CrossRefGoogle Scholar
  60. 60.
    Camp EF, Smith DJ, Evenhuis C, Enochs I, Manzello D, Woodcock S, et al. Acclimatization to high-variance habitats does not enhance physiological tolerance of two key Caribbean corals to future temperature and pH. Proc R Soc Lond B Biol Sci. 2016;283:20160442.CrossRefGoogle Scholar
  61. 61.
    Johnson MD, Moriarty VW, Carpenter RC. Acclimatization of the crustose coralline alga Porolithon onkodes to variable pCO2. PLoS One. 2014;9:e87678.CrossRefGoogle Scholar
  62. 62.
    Dufault AM, Cumbo VR, Fan T-Y, Edmunds PJ. Effects of diurnally oscillating pCO2 on the calcification and survival of coral recruits. Proc R Soc Lond B Biol Sci. 2012;279:2951–8.CrossRefGoogle Scholar
  63. 63.
    Cornwall CE, Hepburn CD, McGraw CM, Currie KI, Pilditch CA, Hunter KA, et al. Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc R Soc Lond B Biol Sci. 2013;280:20132201.CrossRefGoogle Scholar
  64. 64.
    Mayfield AB, Chan P-H, Putnam HM, Chen C-S, Fan T-Y. The effects of a variable temperature regime on the physiology of the reef-building coral Seriatopora hystrix: results from a laboratory-based reciprocal transplant. J Exp Biol. 2012;215:4183–95.CrossRefGoogle Scholar
  65. 65.
    Putnam HM, Edmunds PJ, Fan T-Y. Effect of a fluctuating thermal regime on adult and larval reef corals. Invertebr Biol. 2010;129:199–209.CrossRefGoogle Scholar
  66. 66.
    Putnam HM, Edmunds PJ. The physiological response of reef corals to diel fluctuations in seawater temperature. J Exp Mar Biol Ecol. 2011;396:216–23.CrossRefGoogle Scholar
  67. 67.
    Putnam HM, Edmunds PJ. Responses of coral hosts and their algal symbionts to thermal heterogeneity. Fort Lauderdale: Proc 11th Int. Coral Reef Symp; 2008.Google Scholar
  68. 68.
    Takahashi S, Murata N. How do environmental stresses accelerate photoinhibition? Trends Plant Sci. 2008;13:178–82.CrossRefGoogle Scholar
  69. 69.
    Comeau S, Cornwall CE. Contrasting effects of ocean acidification on coral reefs “animal forests” versus seaweed “kelp forests”. In: Rosi S, editor. Marine Animal Forests. Switzerland: Springer; 2016. p. 1–25.Google Scholar
  70. 70.
    Cornwall CE, Boyd PW, McGraw CM, Hepburn CD, Pilditch CA, Morris JN, et al. Diffusion boundary layers meliorate the negative effects of ocean acidification on the temperate coralline macroalga Arthrocardia corymbosa. PLoS One. 2014;9:e97235.CrossRefGoogle Scholar
  71. 71.
    Raven JA. Implications of inorganic carbon utilization: ecology, evolution, and geochemistry. Can J Bot. 1991;69:908–24.CrossRefGoogle Scholar
  72. 72.
    Raven J. Inorganic carbon acquisition by marine autotrophs. Adv Bot Res. 1997;27:85–209.CrossRefGoogle Scholar
  73. 73.
    Britton D, Cornwall CE, Revill AT, Hurd CL, Johnson CR. Ocean acidification reverses the positive effects of seawater pH fluctuations on growth and photosynthesis of the habitat-forming kelp, Ecklonia radiata. Sci Rep. 2016;6:26036.CrossRefGoogle Scholar
  74. 74.
    Cornwall CE, Revill AT, Hall-Spencer JM, Milazzo M, Raven JA, Hurd CL. Inorganic carbon physiology underpins macroalgal responses to elevated CO2. Sci Rep. 2017;7:46297.CrossRefGoogle Scholar
  75. 75.
    Camp EF, Nitschke MR, Rodolfo-Metalpa R, Houlbreque F, Gardner SG, Smith DJ, et al. Reef-building corals thrive within hot-acidified and deoxygenated waters. Sci Rep. 2017;7:2434.CrossRefGoogle Scholar
  76. 76.
    Lesser MP. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs. 1997;16:187–92.CrossRefGoogle Scholar
  77. 77.
    Schulz KG, Riebesell U. Diurnal changes in seawater carbonate chemistry speciation at increasing atmospheric carbon dioxide. Mar Biol. 2013;160:1889–99.CrossRefGoogle Scholar
  78. 78.
    Albright R, Mason B, Harrison P, Wallace C, Rose K. Projected near-future levels of temperature and pCO2 reduce coral fertilization success. PLoS One. 2013;8:e56468.CrossRefGoogle Scholar
  79. 79.
    Collins S, Bell G. Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature. 2004;431:566–9.CrossRefGoogle Scholar
  80. 80.
    Kroeker KJ, Kordas RL, Crim RN, Singh GG. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett. 2010;13:1419–34.CrossRefGoogle Scholar
  81. 81.
    Dufault AM, Ninokawa A, Bramanti L. The role of light in mediating the effects of ocean acidification on coral calcification. J Exp Biol. 2013;216:1570–7.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Emily B. Rivest
    • 1
  • Steeve Comeau
    • 2
  • Christopher E. Cornwall
    • 2
  1. 1.Virginia Institute of Marine Science, College of William & MaryGloucester PointUSA
  2. 2.School of Earth Science, Oceans Institute, and Australian Research Council Centre of Excellence for Coral Reef StudiesThe University of Western AustraliaCrawleyAustralia

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