Skip to main content

Advertisement

Log in

Ocean acidification has no effect on thermal bleaching in the coral Seriatopora caliendrum

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

The objective of this study was to test whether elevated pCO2 predicted for the year 2100 (85.1 Pa) affects bleaching in the coral Seriatopora caliendrum (Ehrenberg 1834) either independently or interactively with high temperature (30.5 °C). Response variables detected the sequence of events associated with the onset of bleaching: reduction in the photosynthetic performance of symbionts as measured by maximum photochemical efficiency (F v/F m) and effective photochemical efficiency (ΔF/F m′) of PSII, declines in net photosynthesis (P net) and photosynthetic efficiency (alpha, α), and finally, reduced chlorophyll a and symbiont concentrations. S. caliendrum was collected from Nanwan Bay, Taiwan, and subjected to combinations of temperature (27.7 vs. 30.5 °C) and pCO2 (45.1 vs. 85.1 Pa) for 14 days. High temperature reduced values of all dependent variables (i.e., bleaching occurred), but high pCO2 did not affect Symbiodinium photophysiology or productivity, and did not cause bleaching. These results suggest that short-term exposure to 81.5 Pa pCO2, alone and in combination with elevated temperature, does not cause or affect coral bleaching.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • 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 USA 105:17442–17446

    Article  CAS  PubMed  Google Scholar 

  • Behrenfeld MJ, Prasil O, Kolber ZS, Babin M, Falkowski PG (1998) Compensatory changes in photosystem II electron turnover rates protect photosynthesis from photoinhibition. Photosynth Res 58:259–268

    Article  CAS  Google Scholar 

  • Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, Englebert N, Vermeulen F, Hoegh-Guldberg O (2010) Genetic Divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS ONE 5:e10871

    Article  PubMed Central  PubMed  Google Scholar 

  • Brading P, Warner ME, Davey P, Smith DJ, Achterberg EP, Suggett DJ (2011) Differential effects of ocean acidification on growth and photosynthesis among phylotypes of Symbiodinium (Dinophyceae). Limnol Oceanogr 56:927–938

    Article  CAS  Google Scholar 

  • Caldiera K, Jain AK, Hoffert MI (2003) Climate sensitivity uncertainty and the need for energy without CO2 emission. Science 299:2052–2054

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol 43:209–216

    Article  CAS  Google Scholar 

  • Cosgrove J, Borowitzka MA (2010) Chlrophyll fluorescence terminology: an introduction. In: Suggett DJ, Borowitzka MA, Prášil O (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Developments in Applied Phycology 4:1–17

  • Crawley A, Kline DI, Dunn S, Anthony K, Dove S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biol 16:851–863

    Article  Google Scholar 

  • Dai C-F, Horng S (2009) Scleractinian fauna of Taiwan. National Taiwan University Press, Taipei, The robusta group

    Google Scholar 

  • Dickson AG, Sabine CL, Christian JR (eds) (2007) Guide to best practices for ocean CO2 measurements. PICES special publication 3: North Pacific Marine Science Organization, British Columbia

  • Dufault AM, Ninokawa A, Bramanti L, Cumbo VR, Fan T-Y, Edmunds PJ (2013) The role of light in mediating the effects of ocean acidification on coral calcification. J Exp Biol. doi:10.1242/jeb.080549

  • Dunn SR, Schnitzler CE, Weis VM (2007) Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc R Soc B 274:3079–3085

    Article  PubMed  Google Scholar 

  • Edmunds PJ (2012) Effect of pCO2 on the growth, respiration and photophysiology of massive Porites spp. in Moorea French Polynesia. Mar Biol 159:2149–2160

    Article  CAS  Google Scholar 

  • Edmunds PJ, Davies PS (1988) Post-stimulation of respiration rates in the coral Porites porites. Coral Reefs 7:7–9

    Article  Google Scholar 

  • Falkowski PG, Raven JA (eds) (1997) Aquatic photosynthesis. Blackwell Science, Massachusetts

    Google Scholar 

  • Fangue NA, O’Donnel MJ, Sewell MA, Matson PG, MacPherson AC, Hofmann GE (2010) A laboratory-based experimental system for the study of ocean acidification effects on marine invertebrate larvae. Limnol Oceanogr 8:441–452

    Article  CAS  Google Scholar 

  • Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: Interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65

    Article  Google Scholar 

  • Garcia HE, Gordon LI (1992) Oxygen solubility in seawater: Better fitting equations. Limnol Oceanogr 37:1307–1312

    Article  CAS  Google Scholar 

  • Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biol Bull 182:324–332

    Article  Google Scholar 

  • Gates RD, Bil KY, Muscatine L (1999) The influence of an anthozoan “host factor” on the physiology of a symbiotic dinoflagellate. J Exp Mar Biol Ecol 232:241–259

    Article  Google Scholar 

  • Glynn PW (1983) Extensive ‘bleaching’ and death of reef corals on the Pacific coast of Panamá. Environ Conserv 10:149–154

    Article  Google Scholar 

  • Glynn PW (1996) Coral reef bleaching: Facts, hypotheses and implications. Global Change Biol 2:495–509

    Article  Google Scholar 

  • Godinot C, Houlbrèque F, Grover R, Ferrier-Pagès C (2011) Coral uptake of inorganic phosphorus and nitrogen negatively affected by simultaneous changes in temperature and pH. PLoS ONE 6:e25024

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goiran C, Al-Moghrabi S, Allemand D, Jaubert J (1996) Inorganic carbon uptake for photosynthesis by symbiotic coral/dino-flagellate associations. I. Photosynthetic performances of symbionts and dependence on sea water bicarbonate. J Exp Mar Biol Ecol 199:207–225

    Article  CAS  Google Scholar 

  • Herfort L, Thake B, Taubner I (2008) Bicarbonate stimulation of calcification and photosynthesis in two hermatypic corals. J Phycol 44:91–98

    Article  CAS  Google Scholar 

  • Hill R, Ralph PJ (2008) Dark-induced reduction of the plastoquinone pool in zooxanthellae of scleractinian corals and implications for measurements of chlorophyll a fluorescence. Symbiosis 46:45–56

    CAS  Google Scholar 

  • Hill R, Frankart C, Ralph P (2005) Impact of bleaching conditions on the components of non-photochemical quenching in the zooxanthellae of a coral. J Exp Mar Biol Ecol 322:83–92

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Article  Google Scholar 

  • Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Prog Ser 183:73–86

    Article  Google Scholar 

  • Hoegh-Guldberg O, Smith GJ (1989) Influence of the population density of zooxanthellae and supply of ammonium on the biomass and metabolic characteristics of the reef corals Seriatopora hystrix and Stylophora pistillata. Mar Ecol Prog Ser 57:173–186

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89:10302–10305

    Article  CAS  PubMed  Google Scholar 

  • Iguchi A, Ozaki S, Nakamura T, Inoue M, Tanaka Y, Suzuki A, Kawahata H, Sakai K (2011) Effects of acidified seawater on coral calcification and symbiotic algae on the massive coral Porites australiensis. Mar Environ Res 73:32–36

    Article  PubMed  Google Scholar 

  • Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547

    Article  CAS  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c 1 and c 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanzen 167:191–194

    CAS  Google Scholar 

  • Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant, Cell Environ 21:1219–1230

    Article  CAS  Google Scholar 

  • Langdon C, Atkinson MJ (2005) Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res. doi:10.1029/2004JC002576

  • Leclercq N, Gattuso J-P, Jaubert J (2002) Primary production, respiration, and calcification of a coral reef mesocosm under increased CO2 partial pressure. Limnol Oceanogr 47:558–564

    Article  CAS  Google Scholar 

  • Leggat W, Badger MR, Yellowlees D (1999) Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol 121:1247–1255

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192

    Article  Google Scholar 

  • Lesser MP, Weis VM, Patterson MR, Jokiel PL (1994) Effects of morphology and water motion on carbon delivery and productivity in the reef coral, Pocillopora damicornis (Linnaeus): Diffusion barriers, inorganic carbon limitation, and biochemical plasticity. J Exp Mar Biol Ecol 178:153–179

    Article  CAS  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

    Article  Google Scholar 

  • Meehl GA, Arblaster JM, Tebaldi C (2007) Contributions of natural and anthropogenic forcing to changes in temperature extremes over the United States. Geophys Res Lett 34:L19709

    Article  Google Scholar 

  • Muscatine L, Falkowski PG, Porter JW, Dubinsky Z (1984) Fate of photosynthetic fixed carbon in light-and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc Lond B 222:181–202

    Article  CAS  Google Scholar 

  • Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422

    Article  CAS  PubMed  Google Scholar 

  • Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701

    Google Scholar 

  • Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc R Soc B. doi:10.1098/rspb.2012.1454

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Ragni M, Airs RL, Hennige SJ, Suggett DJ, Warner ME, Geider RJ (2010) PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes. Mar Ecol Prog Ser 405:57–70

    Article  Google Scholar 

  • Raven J (2005) Ocean acidification due to increasing atmospheric carbon dioxide. The Royal Society http://royalsociety.org/uploadedFiles/Royal_Society_Content/policy/publications/2005/9634.pdf

  • Reynaud S, Leclercq N, Romaine-Lioud S, Ferrier-Pagès C, Jaubert J, Gattuso J-P (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Global Change Biol 9:1660–1668

    Article  Google Scholar 

  • Schneider K, Erez J (2006) The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol Oceanogr 51:1284–1293

    Article  CAS  Google Scholar 

  • Sebens KP, Johnson AS (1991) Effects of water movement on prey capture and distribution of reef corals. Hydrobiologia 226:91–101

    Article  Google Scholar 

  • Smith DJ, Suggett DJ, Baker NR (2005) Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Global Change Biol 11:1–11

    Article  Google Scholar 

  • Stimson J, Kinzie RA (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen-enrichment and control conditions. J Exp Mar Biol Ecol 153:63–74

    Article  Google Scholar 

  • Suggett DJ, Dong LF, Lawson T, Lawrenz E, Torres L, Smith DJ (2013) Light availability determines susceptibility of reef building corals to ocean acidification. Coral Reefs 32:327–337

    Article  Google Scholar 

  • van Vuuren DP, Edmonds J, Kainuma M, Riahi K, Tomson A, Hibbard K, Hurtt GC, Kram T, Krey V, Lamarque J-F, Masui T, Meinshausen M, Nakicenovic N, Smith SJ, Rose SK (2011) The representative concentration pathways: an overview. Climatic Change 109:5–31

    Article  Google Scholar 

  • Venn AA, Tambutté E, Lotto S, Zoccola D, Allemand D, Tambutté S (2009) Imaging intracellular pH in a reef coral and symbiotic anemone. Proc Natl Acad Sci USA 106:16574–16579

    Article  CAS  PubMed  Google Scholar 

  • Wall CB, Edmunds PJ (2013) In situ effects of low pH and elevated HCO3 on juvenile massive Porites spp. in Moorea, French Polynesia. Bio Bull (in press)

  • Warner ME, Fitt WK, Schmidt GW (1996) The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach. Plant, Cell Environ 19:291–299

    Article  Google Scholar 

  • Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc Natl Acad Sci USA 96:8012–8807

    Google Scholar 

  • Warner ME, Lesser MP, Ralph PJ (2010) Chlorophyll fluorescence in reef building corals. In: Suggett DJ, Borowitzka MA, Prášil O (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Developments in Applied Phycology 4:209–222

  • Weis VM, Smith GJ, Muscatine L (1989) A CO2 supply mechanism in zooxanthellae cnidarians: role of carbonic anhydrase. Mar Biol 100:195–202

    Article  CAS  Google Scholar 

  • Wilkinson C (ed) (2008) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network, Townsville

    Google Scholar 

Download references

Acknowledgments

This research was funded by the US National Science Foundation through Grant BIO-OCE 08-44785 (to PJE) and was submitted in partial fulfillment of the MS degree for CBW. We thank two anonymous reviewers for comments that improved an earlier draft of this paper, V.R. Cumbo, A.M. Dufault, E. Rivest and S. Zamudio for field assistance, and NMMBA for logistical support. This is contribution number 200 of the Marine Biology Program of California State University, Northridge.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. B. Wall.

Additional information

Communicated by Biology Editor Dr. Anastazia Banaszak

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wall, C.B., Fan, TY. & Edmunds, P.J. Ocean acidification has no effect on thermal bleaching in the coral Seriatopora caliendrum . Coral Reefs 33, 119–130 (2014). https://doi.org/10.1007/s00338-013-1085-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-013-1085-2

Keywords

Navigation