Coral Reefs

, Volume 33, Issue 1, pp 15–27 | Cite as

Differential thermal bleaching susceptibilities amongst coral taxa: re-posing the role of the host

Report

Abstract

It is well established that different coral species have different susceptibilities to thermal stress, yet it is less clear which biological or physical mechanisms allow some corals to resist thermal stress, whereas other corals bleach and die. Although the type of symbiont is clearly of fundamental importance, many aspects of coral bleaching cannot be explained solely by differences in symbionts amongst coral species. Here, I use the CO2 (sink) limitation model of coral bleaching to repose various host traits believed to influence thermal tolerance (e.g. metabolic rates, colony tissue thickness, skeletal growth form, mucus production rates, tissue concentration of fluorescent pigments and heterotrophic feedings capacity) in terms of an integrated strategy to reduce the likelihood of CO2 limitation around its intracellular photosymbionts. Contrasting observational data for the skeletal vital effect on oxygen isotope composition (δ18O) partitions two alternate evolutionary strategies. The first strategy is heavily reliant on a sea water supply chain of CO2 to supplement respiratory CO2(met). In contrast, the alternate strategy is less reliant on the sea water supply source, potentially facilitated by increased basal respiration rates and/or a lower photosynthetic demand for CO2. The comparative vulnerability of these alternative strategies to modern ocean conditions is used to explain the global-wide observation that corals with branching morphologies (and thin tissue layers) are generally more thermally sensitive than corals with massive morphologies (and thick tissue layers). The life history implications of this new framework are discussed in terms of contrasting fitness drivers and past environmental constraints, which delivers ominous predictions for the viability of thin-tissued branching and plating species during the present human-dominated (“Anthropocene”) era of the Earth System.

Keywords

CO2 limitation Coral bleaching Respiration Photoinhibition Vital effects Ocean acidification Zooxanthellae density 

References

  1. 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 105:17442–17446PubMedCrossRefGoogle Scholar
  2. Al-Horani FA, Al-Moghrabi SM, De Beer D (2003a) Microsensor study of photosynthesis and calcification in the scleractinian coral, Galaxea fascicularis: active internal carbon cycle. J Exp Mar Biol Ecol 288:1–15CrossRefGoogle Scholar
  3. 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 142:419–426Google Scholar
  4. Al-Moghrabi S, Gorian C, Allemand D, Speziale N, Jaubert J (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral-dinoflagellate association II. Mechanisms for bicarbonate uptake. J Exp Mar Biol Ecol 199:227–248CrossRefGoogle Scholar
  5. Aronson RB, Macintyre IG, Wapnick CM, O’Neill MW (2004) Phase shifts, alternative states, and unprecedented convergence of two reef systems. Ecology 85:1876–1891CrossRefGoogle Scholar
  6. Baghooli R (2013) Inhibition of Calvin-Benson cycle suppresses the repair of Photosystem II in Symbiodinium: implications for coral bleaching. Hydrobiologia 714:183–190CrossRefGoogle Scholar
  7. Baird AH, Hughes TP (2000) Competitive dominance by tabular corals: an experimental analysis of recruitment and survival of understory assemblages. J Exp Mar Biol Ecol 251:117–132PubMedCrossRefGoogle Scholar
  8. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc B 273:2305–2312PubMedCrossRefGoogle Scholar
  9. Bertucci A, Moya A, Tambutte S, Allemand D, Supuran CT, Zoccola D (2013) Carbonic anhydrases in anthozoan corals – A review. Bioorg Med Chem 21:1437–1450PubMedCrossRefGoogle Scholar
  10. Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327CrossRefGoogle Scholar
  11. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:s129–s138CrossRefGoogle Scholar
  12. Buxton L, Badger M, Ralph P (2009) Effects of moderate heat stress and dissolved inorganic carbon concentration on photosynthesis and respiration of Symbiodinium sp. (Dinophyceae) in culture and symbiosis. J Phycol 45:357–365CrossRefGoogle Scholar
  13. Buxton L, Takahashi S, Hill R, Ralph PJ (2012) Variability in the primary site of photosynthesis damage in Symbiodinium sp. (Dinophyceae) exposed to thermal stress. J Phycol 48:117–126CrossRefGoogle Scholar
  14. Castillo KD, Helmuth BST (2005) Influence of thermal history on the response of Montastraea annularis to short-term temperature exposure. Mar Biol 148:261–270CrossRefGoogle Scholar
  15. Cooper TF, Ulstrup KE, Dandan SS, Heyward AJ, Kühl M, Muirhead A, O’Leary RA, Ziersen BEF, van Oppen MJH (2011) Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types. Proc Biol Sci 278:1840–1850PubMedCentralPubMedCrossRefGoogle Scholar
  16. 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 16:851–863CrossRefGoogle Scholar
  17. Cunning R, Baker AC (2013) Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nature Climate Change 3:259–262CrossRefGoogle Scholar
  18. Darling ES, Alvarez-Filip L, Oliver TA, McClanahan TR, Cote IM (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386PubMedCrossRefGoogle Scholar
  19. Diamond JL, Holzman BJ, Bingham BL (2012) Thicker host tissues moderate light stress in a cnidarian endosymbiont. J Exp Biol 215:2247–2254CrossRefGoogle Scholar
  20. Edmunds PJ (2012) Effect of pCO2 on the growth, respiration, and photophysiology of massive Porites spp. in Moorea. French Polynesia. Mar Biol 159:2149–2160CrossRefGoogle Scholar
  21. Enriquez S, Mendez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032CrossRefGoogle Scholar
  22. Finelli CM, Helmuth BST, Pentcheff ND, Wethey DS (2006) Water flow influences oxygen transport and photosynthetic efficiency in corals. Coral Reefs 25:47–57CrossRefGoogle Scholar
  23. Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, Grottoli AG, Gomez M, Fisher P, Lajuenesse TC, Pantos O, Iglesias-Prieto R, Franklin DJ, Rodrigues LJ, Torregiani JM, van Woesik R, Lesser MP (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. J Exp Mar Biol Ecol 373:102–110CrossRefGoogle Scholar
  24. Franklin DJ, Molina Cedrese CM, Hoegh-Guldberg O (2006) Increased mortality and photoinhibition in the symbiotic dinoflagellates of the Indo-Pacific coral Stylophora pistillata (Esper) after summer bleaching. Mar Biol 149:633–642CrossRefGoogle Scholar
  25. Furla P, Allemand D, Orsenigo MN (2000a) Involvement of H+-ATPase and carbonic anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. Am J Physiol Regul Integr Comp Physiol 278:870–881Google Scholar
  26. Furla P, Galgani I, Durand I, Allemand D (2000b) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457PubMedGoogle Scholar
  27. Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43Google Scholar
  28. Gleason DF, Wellington GM (1993) Ultraviolet radiation and coral bleaching. Nature 365:836–838CrossRefGoogle Scholar
  29. Goiran C, Al-Moghrabi S, Allemand D, Jaubert J (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral/dinoflagellate association I. Photosynthetic performances of symbionts and dependence on sea water bicarbonate. J Exp Mar Biol Ecol 199:207–225CrossRefGoogle Scholar
  30. Greenstein BJ, Curran A, Pandolfi JM (1998) Shifting ecological baselines and the demise of Acropora cervicornis in the western North Atlantic and Caribbean Province: a Pleistocene perspective. Coral Reefs 17:249–261CrossRefGoogle Scholar
  31. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189PubMedCrossRefGoogle Scholar
  32. Hennige SJ, Smith DJ, Walsh S, McGinley MP, Warner ME, Suggett DJ (2010) Acclimation and adaptation of scleractinian coral communities along environmental gradients within an Indonesian reef system. J Exp Mar Biol Ecol 391:143–152CrossRefGoogle Scholar
  33. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Nowlton 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 318:1737–1742PubMedCrossRefGoogle Scholar
  34. Hongo C, Yamano H (2013) Species-specific responses of corals to bleaching event on anthropogenically turbid reefs on Okinawa Island, Japan, over a 15-year period (1995-2009). PLoS ONE 8(4):e60952PubMedCentralPubMedCrossRefGoogle Scholar
  35. Johnson KG, Budd AF, Stemann TA (1995) Extinction selectivity and ecology of Neogene Caribbean corals. Paleobiology 21:52–73Google Scholar
  36. Jones RJ, Hoegh-Guldberg O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant Cell Environ 24:89–99CrossRefGoogle Scholar
  37. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Scheiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230CrossRefGoogle Scholar
  38. Juillet-Leclerc A, Schmidt G (2001) A calibration of the oxygen isotope paleothermometer of coral aragonite from Porites. Geophys Res Lett 28:4135–4138CrossRefGoogle Scholar
  39. LaJeunesse TC, Loh WKW, van Woesik R, Ove Hoegh-Guldberg, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceangr 48:2046–2054CrossRefGoogle Scholar
  40. Lane GA, Dole M (1956) Fractionation of oxygen isotopes during respiration. Science 123:574–576PubMedCrossRefGoogle Scholar
  41. Lang J, Chornesky E (1990) Competition between scleractinian reef corals – a review of mechanisms and effects. In: Dubinsky Z (ed) Ecosystems of the World, Vol 25, Coral Reefs. Elsevier, Amsterdam, Netherlands, pp 133–207Google Scholar
  42. Lang JC, Deslarzes KJP, Schmahl GP (2001) The Flower Garden Banks: Remarkable reefs in the NW Gulf of Mexico. Coral Reefs 20:126CrossRefGoogle Scholar
  43. Leggat W, Marendy EM, Baillie B, Whitney SM, Ludwig M, Badger MR, Yellowlees D (2002) Dinoflagellate symbioses: strategies and adaptations for the acquisition and fixation of inorganic carbon. Funct Plant Biol 29:309–322CrossRefGoogle Scholar
  44. Lesser MP (1996) Exposure of symbiotic dinoflagellates to elevated temperatures and ultraviolet radiation causes oxidative stress and inhibits photosynthesis. Limnol Oceanogr 41:271–283CrossRefGoogle Scholar
  45. Levas SJ, Grottoli AG, Hughes A, Osburn CL, Matsui Y (2013) Physiological and biogeochemical traits of bleaching and recovery in the mounding species of coral Porites lobata: implications for resilience in mounding corals. PloS ONE 8:e63267PubMedCentralPubMedCrossRefGoogle Scholar
  46. Levy O, Dubinsky Z, Achituv Y, Erez J (2006) Diurnal polyp expansion behaviour in stony corals may enhance carbon availability for symbiont photosynthesis. J Exp Mar Biol Ecol 333:1–11CrossRefGoogle Scholar
  47. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131CrossRefGoogle Scholar
  48. Madin JS (2005) Mechanical limitations of reef corals during hydrodynamic disturbances. Coral Reefs 24:630–635CrossRefGoogle Scholar
  49. McClanahan TR (2004) The relationship between bleaching and mortality of common corals. Mar Biol 144:1239–1245CrossRefGoogle Scholar
  50. McConnaughey T (1989) 13C and 18O isotopic disequilibrium in biological carbonates: I. Patterns. Geochim Cosmochim Acta 53:151–162Google Scholar
  51. McConnaughey TA, Whelan JF (1997) Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci Rev 42:95–117CrossRefGoogle Scholar
  52. Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163CrossRefGoogle Scholar
  53. Mendes JM, Woodley JD (2002) Effect of the 1995-1996 bleaching event on polyp tissue depth, growth, reproduction, and skeletal band formation in Montastraea annularis. Mar Ecol Prog Ser 235:93–102CrossRefGoogle Scholar
  54. Montaggioni LF (2005) History of Indo-Pacific coral reef systems since the last glaciation: Development patterns and controlling factors. Earth Sci Rev 71:1–75CrossRefGoogle Scholar
  55. Muscatine L, Porter JW, Kaplan IR (1989) Resource partitioning by reef corals as determined from stable isotope composition: I. δ13C of zooxanthellae and animal tissue vs. depth. Mar Biol 100:185–193CrossRefGoogle Scholar
  56. Muscatine L, Ferrier-Pages C, Blackburn A, Gates RD, Baghdasarian G, Allemand D (1998) Cell-specific density of symbiotic dinoflagellates in tropical anthozoans. Coral Reefs 17:329–337CrossRefGoogle Scholar
  57. Nakamura T, van Woesik R, Yamasaki H (2005) Photoinhibition of photosynthesis is reduced by water flow in the reef-building coral Acropora digitifera. Mar Ecol Prog Ser 301:109–118CrossRefGoogle Scholar
  58. Pandolfi JM, Jackson JBC (2006) Ecological persistence interrupted in Caribbean coral reefs. Ecol Lett 9:818–826PubMedCrossRefGoogle Scholar
  59. Pearson PN, Palmer MR (2000) Atmospheric carbon dioxide concentrations over the past 60 million years. Nature 406:695–699PubMedCrossRefGoogle Scholar
  60. Porter JW (1976) Autotrophy, heterotrophy, and resource partitioning in Caribbean reef building corals. Am Nat 110:731–742CrossRefGoogle Scholar
  61. Reynaud-Vaganay S, Juillet-Leclerc A, Jaubert J, Gattuso J-P (2001) Effect of light on skeletal δ13C and δ18O, and interaction with photosynthesis, respiration and calcification in two zooxanthellate scleractinian corals. Palaeogeogr Palaeoclim Palaeoecol 175:393–404CrossRefGoogle Scholar
  62. Richman S, Loya Y, Slobodkin LB (1975) The rate of mucus production by corals and its assimilation by the coral reef copepod Acartia negligens. Limnol Oeanogr 20:918–923CrossRefGoogle Scholar
  63. Rollion-Bard C, Blamart D, Cuif JP, Dauphin Y (2010) In situ measurements of oxygen isotopic composition in deep-sea coral, Lophelia pertusa: Re-examination of the current geochemical models of biomineralization. Geochim Cosmochim Acta 74:1338–1349CrossRefGoogle Scholar
  64. Rowan R, Whitney SM, Fowler A, Yellowlees D (1996) Rubisco in marine symbiotic dinoflagellates: Form II enzyme in eukaryotic oxygenic phototrophs encoded by a nuclear encoded multigene family. Plant Cell 8:539–553PubMedCentralPubMedGoogle Scholar
  65. Salih A, Hoegh-Guldberg O, Cox G (1998) Photoprotection of symbiotic dinoflagellates by fluorescent pigments in reef corals. In: Greenwood JG, Hall NJ (eds) Australian Coral Reef Society 75th Anniversary Conference. The Univ of Queensland, pp 217–230Google Scholar
  66. Shyka TA, Sebens KP (2000) Community structure, water column nutrients, and water flow in two Pelican Cays ponds, Belize. Atoll Res Bull 471:105–121CrossRefGoogle Scholar
  67. Smith FA, Walker NA (1980) Photosynthesis by aquatic plants: effects of unstirred layers in relation to assimilation of CO2 and HCO3- and to carbon isotopic discrimination. New Phytol 86:245–259CrossRefGoogle Scholar
  68. Swart PK (1983) Carbon and oxygen isotope fractionation in scleractinian corals: a Review. Earth Sci Rev 19:51–80CrossRefGoogle Scholar
  69. Tremblay P, Grover R, Maguer JF, Legendre L, Ferrier-Pagès C (2012) Autotrophic carbon budget in coral tissue: a new 13C-based model of photosynthate translocation. J Exp Biol 215:1384–1393PubMedCrossRefGoogle Scholar
  70. Trench RK (1993) Microalgal-invertebrate symbioses: a review. Endocytobiosis and Cell Research 9:135–175Google Scholar
  71. Uchikawa J, Zeebe RE (2012) The effect of carbonic anhydrase on the kinetics and equilibrium of the oxygen isotope exchange in the CO2-H2O system: Implications for δ18O vital effects in biogenic carbonates. Geochim Cosmochim Acta 95:15–34CrossRefGoogle Scholar
  72. Ulstrup KE, Kühl M, van Oppen MJH, Cooper TF, Ralph PJ (2011) Variation in photosynthesis and respiration in geographically distinct populations of two reef-building coral species. Aquat Biol 12:241–248CrossRefGoogle Scholar
  73. van Woesik R, Franklin EC, O’Leary J, McClanahan TR, Klaus JS, Budd AF (2012) Hosts of the Plio-Pleistocene past reflect modern-day coral vulnerability. Proc R Soc B 279:2448–2456PubMedCrossRefGoogle Scholar
  74. Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  75. Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Nat Acad Sci USA 96:8007–8012PubMedCrossRefGoogle Scholar
  76. Weber JN, Woodhead PMJ (1970) C and O isotope fractionation in the skeletal carbonate of reef-building corals. Chem Geol 6:93–117CrossRefGoogle Scholar
  77. Weber JN, Woodhead PMJ (1972a) Temperature dependence of oxygen-18 concentration in reef coral carbonates. J Geophys Res 77:463–473CrossRefGoogle Scholar
  78. Weber JN, Woodhead PMJ (1972b) Stable isotope ratio variations in non-scleractinian coelenterate carbonates as a function of temperature. Mar Biol 15:293–297CrossRefGoogle Scholar
  79. Weis VM, Smith GJ, Muscatine L (1989) A “CO2 supply” mechanism in zooxanthellate cnidarians: role of carbonic anhydrase. Mar Biol 100:195–202CrossRefGoogle Scholar
  80. Wells JW (1959) Notes on Indo-Pacific Scleractinian corals parts I and II: part I. Oryzotrochus, a new genus of Turbinolian coral. Pac Sci 13:286–290Google Scholar
  81. Woods R (1999) Reef evolution. Oxford Univ Press, New York, USAGoogle Scholar
  82. Wooldridge SA (2009a) A new conceptual model for the warm-water breakdown of the coral-algae endosymbiosis. Mar Freshw Res 60:483–496CrossRefGoogle Scholar
  83. Wooldridge SA (2009b) A new conceptual model for the enhanced release of mucus in symbiotic reef corals during ‘bleaching’ conditions. Mar Ecol Prog Ser 396:145–152CrossRefGoogle Scholar
  84. Wooldridge SA (2010) Is the coral-algae symbiosis really mutually-beneficial for the partners? BioEssays 32:615–625PubMedCrossRefGoogle Scholar
  85. Wooldridge SA (2012) A hypothesis linking sub-optimal seawater pCO2 conditions for cnidarians-Symbiodinium symbioses with the exceedence of the interglacial threshold (> 260 ppmv). Biogeosciences 9:1709–1723CrossRefGoogle Scholar
  86. Wooldridge SA (2013a) Breakdown of the coral-algae symbiosis: towards formalising a linkage between warm-water bleaching thresholds and the growth rate of the intracellular zooxanthellae. Biogeosciences 10:1647–1658CrossRefGoogle Scholar
  87. Wooldridge SA (2013b) A new conceptual model of coral biomineralisation: hypoxia as the physiological driver of skeletal extension. Biogeosciences 10:2867–2884CrossRefGoogle Scholar
  88. Yee SH, Santavy DL, Barron MG (2008) Comparing environmental influences on coral bleaching across and within species using clustered binomial regression. Ecol Model 24:162–174CrossRefGoogle Scholar
  89. Yellowlees D, Rees TA, Leggat W (2008) Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ 31:679–694PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Australian Institute of Marine ScienceTownsvilleAustralia

Personalised recommendations