Advertisement

Coral Reefs

, Volume 37, Issue 4, pp 1169–1180 | Cite as

Impacts of coral bleaching on pH and oxygen gradients across the coral concentration boundary layer: a microsensor study

  • Verena Schoepf
  • Christopher E. Cornwall
  • Svenja M. Pfeifer
  • Steven A. Carrion
  • Cinzia Alessi
  • Steeve Comeau
  • Malcolm T. McCulloch
Report

Abstract

Reef-building corals are surrounded by complex microenvironments (i.e. concentration boundary layers) that partially isolate them from the ambient seawater. Although the presence of such concentration boundary layers (CBLs) could potentially play a role in mitigating the negative impacts of climate change stressors, their role is poorly understood. Furthermore, it is largely unknown how heat stress-induced bleaching affects O2 and pH dynamics across the CBLs of coral, particularly in branching species. We experimentally exposed the common coral species Acropora aspera to heat stress for 13 d and conducted a range of physiological and daytime microsensor measurements to determine the effects of bleaching on O2 and pH gradients across the CBL. Heat stress equivalent to 24 degree heating days (3.4 degree heating weeks) resulted in visible bleaching and significant declines in photochemical efficiency, photosynthesis rates and photosynthesis to respiration (P/R) ratios, whereas dark respiration and calcification rates were not impacted. As a consequence, bleached A. aspera had significantly lower (− 13%) surface O2 concentrations during the day than healthy corals, with concentrations being lower than that of the ambient seawater, thus resulting in O2 uptake from the seawater. Furthermore, we show here that Acropora, and potentially branching corals in general, have among the lowest surface pH elevation of all corals studied to date (0.041 units), which could contribute to their higher sensitivity to ocean acidification. Additionally, bleached A. aspera no longer elevated their surface pH above ambient seawater values and, therefore, had essentially no [H+] CBL. These findings demonstrate that heat stress-induced bleaching has negative effects on pH elevation and [H+] CBL thickness, which may increase the overall susceptibility of coral to the combined impacts of ocean acidification and warming.

Keywords

Acropora aspera Metabolism Calcification Diffusive oxygen flux Concentration gradients Heat stress 

Notes

Acknowledgements

Funding for this study was provided by the Australian Research Council (ARC) Centre of Excellence for Coral Reef Studies, the Western Australian Marine Science Institution (WAMSI), an ARC Laureate Fellowship awarded to MM and an ARC DECRA Award (DE160100668) awarded to SC.

Compliance with ethical standards

Conflict of interest

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

References

  1. Agostini S, Fujimura H, Higuchi T, Yuyama I, Casareto BE, Suzuki Y, Nakano Y (2013) The effects of thermal and high-CO2 stresses on the metabolism and surrounding microenvironment of the coral Galaxea fascicularis. Comptes Rendus Biologies 336:384–391CrossRefGoogle Scholar
  2. Al-Horani FA (2005) Effects of changing seawater temperature on photosynthesis and calcification in the scleractinian coral Galaxea fascicularis, measured with O2, Ca2+ and pH microsensors. Scientia Marina 69:347–354CrossRefGoogle Scholar
  3. Al-Horani FA, Al-Moghrabi SM, De Beer D (2003a) Microsensor study of photosynthesis and calcification in the sceractinian coral, Galaxea fascicularis: active internal carbon cycle. J Exp Mar Biol Ecol 288:1–15CrossRefGoogle Scholar
  4. Al-Horani FA, Al-Moghrabi SM, de Beer D (2003b) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426CrossRefGoogle Scholar
  5. Baird A, Marshall P (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141CrossRefGoogle Scholar
  6. 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 Comm 7:11144CrossRefGoogle Scholar
  7. Chan NCS, Wangpraseurt D, Kühl M, Connolly S (2016) Flow and coral morphology control coral surface pH: Implications for the effects of ocean acidification. Frontiers in Marine Science 3: https://doi.org/10.3389/fmars.2016.00010
  8. Cornwall CE, Hepburn CD, Pilditch CA, Hurd CL (2013) Concentration boundary layers around complex assemblages of macroalgae: Implications for the effects of ocean acidification on understory coralline algae. Limnol Oceanogr 58:121–130CrossRefGoogle Scholar
  9. Cornwall CE, Boyd PW, McGraw CM, Hepburn CD, Pilditch CA, Morris JN, Smith AM, Hurd CL (2014) Diffusion boundary layers ameliorate the negative effects of ocean acidification on the temperate coralline macroalga Arthrocardia corymbosa. PLoS One 9:e97235CrossRefGoogle Scholar
  10. D’Olivo JP, McCulloch MT (2017) Response of coral calcification and calcifying fluid composition to thermally induced bleaching stress. Sci Rep 7:2207CrossRefGoogle Scholar
  11. 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 34:1151–1163CrossRefGoogle Scholar
  12. de Beer D, Kühl M, Stambler N, Vaki L (2000) A microsensor study of light enhanced Ca2+ uptake and photosynthesis in the reef-building hermatypic coral Favia sp. Mar Ecol Prog Ser 194:75–85CrossRefGoogle Scholar
  13. Dickson AG, Sabine CL, Christian JR (2007) Guide to Best Practices for Ocean CO2 Measurements. PICES Special Publication 3:191 ppGoogle Scholar
  14. Edmunds PJ, Brown D, Moriarty V (2012) Interactive effects of ocean acidification and temperature on two scleractinian corals from Moorea, French Polynesia. Global Change Biol 18:2173–2183CrossRefGoogle Scholar
  15. Enríquez S, Méndez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032CrossRefGoogle Scholar
  16. Garcia HE, Gordon LI (1992) Oxygen solubility in seawater: Better fitting equations. Limnol Oceanogr 37:1307–1312CrossRefGoogle Scholar
  17. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189CrossRefGoogle Scholar
  18. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck R, 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 318:1737–1742CrossRefGoogle Scholar
  19. 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 359:80–83CrossRefGoogle Scholar
  20. 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 J-PA, Hoogenboom MO, Kennedy EV, C-y Kuo, 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 543:373–377CrossRefGoogle Scholar
  21. Hurd CL (2015) Slow-flow habitats as refugia for coastal calcifiers from ocean acidification. J Phycol 51:599–605CrossRefGoogle Scholar
  22. Hurd CL, Cornwall CE, Currie K, Hepburn CD, McGraw CM, Hunter KA, Boyd PW (2011) Metabolically induced pH fluctuations by some coastal calcifiers exceed projected 22nd century ocean acidification: a mechanism for differential susceptibility? Global Change Biol 17:3254–3262CrossRefGoogle Scholar
  23. IPCC (2013) Climate Change 2013: The physical science basis. Summary for Policy Makers., http://www.ipcc.ch website
  24. Jamieson D, Chance B, Cadenas E, Boveris A (1986) The relation of free radical production to hyperoxia. Annual Review of Physiology 48:703–719CrossRefGoogle Scholar
  25. Jimenez IM, Kühl M, Larkum AWD, Ralph PJ (2011) Effects of flow and colony morphology on the thermal boundary layer of corals. J R Soc Interface 8:1785–1795CrossRefGoogle Scholar
  26. Jokiel PL, Maragos JE, Franzisket L (1978) Coral growth: buoyant weight technique. In: Stoddart DR, Johannes RE (eds) Coral Reefs: Resesarch Methods. UNESCO, Paris, pp 529–541Google Scholar
  27. Jorgensen BB, Revsbech NP (1985) Diffusive boundary layers and the oxygen uptake of sediments and detritus. Limnol Oceanogr 30:112–122Google Scholar
  28. Koren K, Jakobsen SL, Kühl M (2016) In-vivo imaging of O2 dynamics on coral surfaces spray-painted with sensor nanoparticles. Sensors and Actuators B: Chemical 237:1095–1101CrossRefGoogle Scholar
  29. Kühl M, Cohen Y, Dalsgaard T, Jorgensen BB, Revsbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and Light. Mar Ecol Prog Ser 117:159–172CrossRefGoogle Scholar
  30. Legendre P, Legendre L (1998) Numerical Ecology. ElsevierGoogle Scholar
  31. Maynard JA, Turner PJ, Anthony KRN, Baird AH, Berkelmans R, Eakin CM, Johnson J, Marshall PA, Packer GR, Rea A, Willis BL (2008) ReefTemp: An interactive monitoring system for coral bleaching using high-resolution SST and improved stress predictors. Geophys Res Lett 35:L05603CrossRefGoogle Scholar
  32. McCulloch MT, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Change 2:623–627CrossRefGoogle Scholar
  33. Nishihara GN, Ackerman JD (2007) On the determination of mass transfer in a concentration boundary layer. Limnol Oceanogr Meth 5:88–96CrossRefGoogle Scholar
  34. NOAA (2016) NOAA Coral Reef Watch Climatology version 2 NOAA Coral Reef Watch: MethodologyGoogle Scholar
  35. Noisette F, Hurd C (2018) Abiotic and biotic interactions in the diffusive boundary layer of kelp blades create a potential refuge from ocean acidification. Funct Ecol 32:1329–1342CrossRefGoogle Scholar
  36. Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke RG, McArdle D, McClenachan L, Newman MJH, Paredes G, Warner RR, Jackson JBC (2003) Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958CrossRefGoogle Scholar
  37. Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882CrossRefGoogle Scholar
  38. Schoepf V, Grottoli AG, Warner M, Cai W-J, Melman TF, Hoadley KD, Pettay DT, Hu X, Li Q, Xu H, Wang Y, Matsui Y, Baumann J (2013) Coral energy reserves and calcification in a high-CO2 world at two temperatures. PLoS One 8:e75049CrossRefGoogle Scholar
  39. 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. PLoS One 9:e112011CrossRefGoogle Scholar
  40. Schoepf V, Stat M, Falter JL, McCulloch MT (2015a) Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment. Sci Rep 5:17639CrossRefGoogle Scholar
  41. Schoepf V, Grottoli AG, Levas SJ, Aschaffenburg MD, Baumann JH, Matsui Y, Warner ME (2015b) Annual coral bleaching and the long-term recovery capacity of coral. Proc R Soc B 282:20151887CrossRefGoogle Scholar
  42. Schoepf V, Jury CP, Toonen RJ, McCulloch MT (2017) Coral calcification mechanisms facilitate adaptive responses to ocean acidification. Proc R Soc B: Biol Sci 284:20172117CrossRefGoogle Scholar
  43. Shashar N, Cohen Y, Loya Y (1993) Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol Bull 185:455–461CrossRefGoogle Scholar
  44. Siebeck UE, Marshall NJ, Klüter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460CrossRefGoogle Scholar
  45. Towle EK, Enochs IC, Langdon C (2015) Threatened Caribbean coral is able to mitigate the adverse effects of ocean acidification on calcification by increasing feeding rate. PLoS One 10:e0123394CrossRefGoogle Scholar
  46. 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 110:1634–1639CrossRefGoogle Scholar
  47. Wangpraseurt D, Larkum AWD, Ralph PJ, Kühl M (2012) Light gradients and optical microniches in coral tissues. Front Microbiol 3: https://doi.org/10.3389/fmicb.2012.00316

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Oceans Graduate School and UWA Oceans InstituteThe University of Western AustraliaPerthAustralia
  2. 2.ARC Centre of Excellence for Coral Reef StudiesThe University of Western AustraliaPerthAustralia
  3. 3.Department of BiologyHeinrich-Heine-Universität DüsseldorfDüsseldorfGermany
  4. 4.School of GeosciencesUniversity of EdinburghEdinburghUK
  5. 5.Department of Earth and Marine Science (DiSTeM)University of PalermoPalermoItaly
  6. 6.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand
  7. 7.Laboratoire d’Océanographie de Villefranche, CNRS-INSUSorbonne UniversitéVillefranche-sur-merFrance

Personalised recommendations