Marine Biology

, Volume 162, Issue 3, pp 717–723 | Cite as

Species-specific differences in thermal tolerance may define susceptibility to intracellular acidosis in reef corals

  • Emma M. Gibbin
  • Hollie M. Putnam
  • Ruth D. Gates
  • Matthew R. Nitschke
  • Simon K. Davy
Short note

Abstract

It is widely acknowledged that temperature stress affects an organism’s sensitivity to ocean acidification and vice versa, yet it is not clear how the two are mechanistically linked. Here, we induced thermal stress in two coral species with differing bleaching susceptibilities to measure how a reduction in photosynthetic performance impacts intracellular pH (pHi) regulation in the symbiotic dinoflagellates (Symbiodinium sp.) and their host coral cells. Our hypothesis was that thermally induced photosynthetic dysfunction in the symbiont would prevent the efficient removal of additional CO2, lowering its buffering capacity and thus increasing the host cell’s susceptibility to intracellular acidosis. To test this, we exposed Pocillopora damicornis (a thermally sensitive coral) and Montipora capitata (a thermally resilient coral) to four different temperature treatments (23.8, 25.5, 28 and 31 °C) for 1 week. We then isolated intact symbiotic coral endodermal cells, placed them in a live-cell chamber attached to a confocal microscope and bathed them in CO2-acidified seawater (~pH 7.6) for 30 min, before measuring the light-adapted pHi of both the host cell and its symbiont. Cells isolated from P. damicornis were more prone to cellular acidosis (declines in pHi of 11 and 8 % in host and symbiont, respectively, at 31 °C relative to 23.8 °C) than cells isolated from M. capitata (5 and 4 %, respectively). These results highlight the important role of Symbiodinium productivity (in addition to a range of physico-chemical factors such as skeletal morphology and tissue pigmentation) in determining the sensitivity of corals to rising sea surface temperatures and ocean acidification.

Supplementary material

227_2015_2617_MOESM1_ESM.pdf (259 kb)
Supplementary material 1 (PDF 259 kb)

References

  1. Anlauf H, D’Croz L, O’Dea A (2011) A corrosive concoction: the combined effects of ocean warming and acidification on the early growth of a stony coral are multiplicative. J Exp Mar Biol Ecol 397:13–20. doi:10.1016/j.jembe.2010.11.009 CrossRefGoogle Scholar
  2. Baird A, Bhagooli R, Ralph P, Takahashi S (2009) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20. doi:10.1016/j.tree.2008.09.005 CrossRefGoogle Scholar
  3. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689. doi:10.1146/132417 CrossRefGoogle Scholar
  4. Bell JJ, Davy SK, Jones T, Taylor MW, Webster NS (2013) Could some coral reefs become sponge reefs as our climate changes? Glob Change Biol 19:2613–2624. doi:10.1111/gcb.12212 CrossRefGoogle Scholar
  5. Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner A, Chiriboga A, Cortés J, Delbeek JC, Devantier L, Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR, Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro BA, Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD, Sanciangco J, Sheppard A, Sheppard C, Smith K, Stuart S, Turak E, Veron JE, Wallace C, Weil Em Wood E (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563. doi:10.1126/science.1159196 CrossRefGoogle Scholar
  6. Casey JR, Grinstein S, Orlowski J (2010) Sensors and regulators of intracellular pH. Nat Rev Mol Cell Bio 11:50–61. doi:10.1038/nrm2820 CrossRefGoogle Scholar
  7. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261. doi:10.1128/mmbr.05014-11 CrossRefGoogle Scholar
  8. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication, vol 3, p 191Google Scholar
  9. Fisher P, Malme M, Dove S (2012) The effect of temperature stress on coral-Symbiodinium associations containing distinct symbiont types. Coral Reefs 31:473–485. doi:10.1007/s00338-011-0853-0 CrossRefGoogle Scholar
  10. Fitt W, Brown B, Warner M, Dunne R (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65. doi:10.1007/s003380100146 CrossRefGoogle Scholar
  11. Gibbin EM, Putnam HM, Davy SK, Gates RD (2014) Intracellular pH and its response to CO2-driven seawater acidification in symbiotic versus non-symbiotic coral cells. J Exp Biol 217:1963–1969. doi:10.1242/jeb.099549 CrossRefGoogle Scholar
  12. IPCC (2014) Summary for policymakers. In: Climate change 2014: impacts, adaptation and vulnerability. Part A: global and sectoral aspects. Contribution of the working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 1–32Google Scholar
  13. Jeffrey S, Humphrey G (1975) New spectrophotometry equations for determining chlorophyll a, chlorophyll b, chlorophyll c-1 and chlorophyll c-2 in higher plants, algae and natural phytoplankton. Biochimie Physiol Pflanzen 167:191–194Google Scholar
  14. Jimenez IM, Kühl M, Larkum AW, Ralph PJ (2011) Effects of flow and colony morphology on the thermal boundary layer of corals. J R Soc Interface 8:1785–1795. doi:10.1098/rsif.2011.0144 CrossRefGoogle Scholar
  15. Jokiel PL, Brown EK (2004) Global warming, regional trends and inshore environmental conditions influence coral bleaching in Hawaii. Glob Change Biol 10:1627–1641. doi:10.1111/j.1365-2486.2004.00836.x CrossRefGoogle Scholar
  16. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso J-P (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19:1884–1896. doi:10.1111/gcb.12179 CrossRefGoogle Scholar
  17. LaJeunesse TC, Thornhill DJ, Cox EF, Stanton FG, Fitt WK, Schmidt GW (2004) High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 23:596–603. doi:10.1007/s00338-004-0428-4 Google Scholar
  18. Laurent J, Venn A, Tambutté É, Ganot P, Allemand D, Tambutté S (2013) Regulation of intracellular pH in cnidarians: response to acidosis in Anemonia viridis. FEBS J 281:683–695. doi:10.1111/febs.12614 CrossRefGoogle Scholar
  19. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278. doi:10.1146/annurev.physiol.68.040104.110001 CrossRefGoogle Scholar
  20. 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. doi:10.1046/j.1461-0248.2001.00203.x CrossRefGoogle Scholar
  21. Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol 15:2089–2100. doi:10.1111/j.1365-2486.2009.01874.x CrossRefGoogle Scholar
  22. McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2:623–633. doi:10.1038/nclimate1473 CrossRefGoogle Scholar
  23. Oliver TA, Palumbi SR (2011) Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30:429–440. doi:10.1007/s00338-011-0721-y CrossRefGoogle Scholar
  24. Padilla-Gamiño JL, Pochon X, Bird C, Concepcion GT, Gates RD (2012) From parent to gamete: vertical transmission of Symbiodinium (Dinophyceae) ITS2 sequence assemblages in the reef building coral Montipora capitata. PLoS ONE 7:e38440. doi:10.1371/journal.pone.0038440 CrossRefGoogle Scholar
  25. Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science 344:895–898. doi:10.1126/science.1251336 CrossRefGoogle Scholar
  26. Pochon X, Gates RD (2010) A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol 56:492–497. doi:10.1016/j.ympev.2010.03.040 CrossRefGoogle Scholar
  27. Pörtner H-O, Peck L, Zielinski S, Conway L (1999) Intracellular pH and energy metabolism in the highly stenothermal Antarctic bivalve Limopsis marionensis as a function of ambient temperature. Polar Biol 22:17–30. doi:10.1007/s003000050386 CrossRefGoogle Scholar
  28. Quinn GR, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  29. Rodolfo-Metalpa R, Martin S, Ferrier-Pagès C, Gattuso J-P (2010) Response of the temperate coral Cladocora caespitosa to mid-and long-term exposure to pCO2 and temperature levels projected in 2100. Biogeosci Discuss 7:289–300. doi:10.5194/bg-7-289-2010 CrossRefGoogle Scholar
  30. Rodolfo-Metalpa R, Houlbrèque F, Tambutté E, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso J-P, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Clim Chang 1:308–312. doi:10.1038/nclimate1200 CrossRefGoogle Scholar
  31. Sartoris F-J, Bock C, Serendero I, Lannig G, Pörtner H-O (2003) Temperature-dependent changes in energy metabolism, intracellular pH and blood oxygen tension in the Atlantic cod. J Fish Biol 62:1239–1253. doi:10.1046/j.1095-8649.2003.00099.x CrossRefGoogle Scholar
  32. Shamberger KE, Cohen AL, Golbuu Y, McCorkle DC, Lentz SJ, Barkley HC (2014) Diverse coral communities in naturally acidified waters of a western Pacific reef. Geophys Res Lett 41:499–504. doi:10.1002/2013GL058489 CrossRefGoogle Scholar
  33. Stimson J, Kinzie RA III (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. doi:10.1016/S0022-0981(05)80006-1 CrossRefGoogle Scholar
  34. 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 106:16574–16579. doi:10.1073/pnas.0902894106 CrossRefGoogle Scholar
  35. Venn AA, Tambutté E, Holcomb M, Laurent J, Allemand D, Tambutté S (2013) Impact of seawater acidification on pH at the tissue-skeleton interface and calcification in reef corals. Proc Nat Acad Sci 110:1634–1639. doi:10.1073/pnas.1216153110 CrossRefGoogle Scholar
  36. Weis VM (2008) Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066. doi:10.1242/jeb.009597 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Emma M. Gibbin
    • 1
  • Hollie M. Putnam
    • 2
  • Ruth D. Gates
    • 2
  • Matthew R. Nitschke
    • 3
  • Simon K. Davy
    • 1
  1. 1.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand
  2. 2.Hawaii Institute of Marine BiologyUniversity of HawaiiKaneoheUSA
  3. 3.School of Biological SciencesThe University of QueenslandBrisbaneAustralia

Personalised recommendations