Coral Reefs

, Volume 34, Issue 4, pp 1229–1241 | Cite as

Antioxidant responses to heat and light stress differ with habitat in a common reef coral

  • Thomas D. Hawkins
  • Thomas Krueger
  • Shaun P. Wilkinson
  • Paul L. Fisher
  • Simon K. Davy


Coral bleaching—the stress-induced collapse of the coral–Symbiodinium symbiosis—is a significant driver of worldwide coral reef degradation. Yet, not all corals are equally susceptible to bleaching, and we lack a clear understanding of the mechanisms underpinning their differential susceptibilities. Here, we focus on cellular redox regulation as a potential determinant of bleaching susceptibility in the reef coral Stylophora pistillata. Using slow heating (1 °C d−1) and altered irradiance, we induced bleaching in S. pistillata colonies sampled from two depths [5–8 m (shallow) and 15–18 m (deep)]. There was significant depth-dependent variability in the timing and extent of bleaching (loss of symbiont cells), as well as in host enzymatic antioxidant activity [specifically, superoxide dismutase and catalase (CAT)]. However, among the coral fragments that bleached, most did so without displaying any evidence of a host enzymatic antioxidant response. For example, both deep and shallow corals suffered significant symbiont loss at elevated temperature, but only deep colonies exposed to high temperature and high light displayed any up-regulation of host antioxidant enzyme activity (CAT). Surprisingly, this preceded the equivalent antioxidant responses of the symbiont, which raises questions about the source(s) of hydrogen peroxide in the symbiosis. Overall, changes in enzymatic antioxidant activity in the symbionts were driven primarily by irradiance rather than temperature, and responses were similar across depth groups. Taken together, our results suggest that in the absence of light stress, heating of 1 °C d−1 to 4 °C above ambient is not sufficient to induce a substantial oxidative challenge in S. pistillata. We provide some of the first evidence that regulation of coral enzymatic antioxidants can vary significantly depending on habitat, and, in terms of determining bleaching susceptibility, our results suggest a significant role for the host’s differential regulation of cellular redox status.


Coral bleaching Cnidarian–dinoflagellate symbiosis Symbiodinium Stylophora pistillata Oxidative stress Climate change 



We wish to thank the staff at Heron Island Research Station, University of Queensland, for their assistance with sampling and equipment maintenance, and Dr Olga Pantos for providing storage space for samples during transit. This work was carried out as part of a PhD project supported by a Commonwealth Scholarship awarded to TH, a Marsden Fund award (#VUW0902) to SKD and PF, a Marsden-funded PhD scholarship to TK, and a Victoria University of Wellington Vice Chancellor’s Strategic Research PhD Scholarship to SPW. Finally, we thank Dr Mark Warner, members of the Davy Lab and four anonymous reviewers for their constructive feedback.

Supplementary material

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Supplementary material 1 (TIFF 199 kb)
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Supplementary material 2 (DOCX 13 kb)
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Supplementary material 3 (DOCX 33 kb)


  1. Armoza-Zvuloni R, Shaked Y (2014) Release of hydrogen peroxide and antioxidants by the coral Stylophora pistillata to its external milieu. Biogeosci Discuss 11:33–59CrossRefGoogle Scholar
  2. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639CrossRefPubMedGoogle Scholar
  3. Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 228–287Google Scholar
  4. Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2008) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20CrossRefPubMedGoogle Scholar
  5. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287CrossRefPubMedGoogle Scholar
  6. Beers R, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140PubMedGoogle Scholar
  7. Bellantuono AJ, Hoegh-Guldberg O, Rodriguez-Lanetty M (2012) Resistance to thermal stress in corals without changes in symbiont composition. Proc R Soc Lond B Biol Sci 279:1100–1107CrossRefGoogle 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 Lond B Biol Sci 273:2305–2312CrossRefGoogle Scholar
  9. 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:e10871PubMedCentralCrossRefPubMedGoogle Scholar
  10. Bowler C, Van Camp W, Van Montagu M, Inze D (1994) Superoxide dismutase in plants. CRC Crit Rev Plant Sci 13:199–218CrossRefGoogle Scholar
  11. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326CrossRefGoogle Scholar
  12. Davy SK, Allemand D, Weis VM (2012) The cell biology of cnidarian–dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261PubMedCentralCrossRefPubMedGoogle Scholar
  13. Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 33:533–543CrossRefPubMedGoogle Scholar
  14. Downs CA, McDougall KE, Woodley CM, Fauth JE, Richmond RH, Kushmaro A, Gibb SW, Loya Y, Ostrander GK, Kramarsky-Winter E (2013) Heat-stress and light-stress induce different cellular pathologies in the symbiotic dinoflagellate during coral bleaching. PLoS One 8:e77173PubMedCentralCrossRefPubMedGoogle Scholar
  15. Dunn SR, Pernice M, Green K, Hoegh-Guldberg O, Dove SG (2012) Thermal stress promotes host mitochondrial degradation in symbiotic cnidarians: are the batteries of the reef going to run out? PLoS One 7:e39024PubMedCentralCrossRefPubMedGoogle Scholar
  16. Dykens JA, Shick JM (1982) Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297:579–580CrossRefGoogle Scholar
  17. Dykens JA, Shick JM (1984) Photobiology of the symbiotic sea anemone, Anthopleura elegantissima: defenses against photodynamic effects, and seasonal photoacclimatization. Biol Bull 167:683–697CrossRefGoogle Scholar
  18. Ernst O, Zor T (2010) Linearization of the Bradford protein assay. J Vis Exp 38:e1918Google Scholar
  19. Fabricius KE (2006) Effects of irradiance, flow, and colony pigmentation on the temperature microenvironment around corals: implications for coral bleaching? Limnol Oceanogr 51:30–37CrossRefGoogle Scholar
  20. Franklin EC, Stat M, Pochon X, Putnam HM, Gates RD (2012) GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium–host symbioses. Mol Ecol Res 12:369–373CrossRefGoogle Scholar
  21. Glynn PW, Mate JL, Baker AC, Calderon MO (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997–1998 El Nino-Southern oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull Mar Sci 69:79–109Google Scholar
  22. Goreau TF (1990) Coral bleaching in Jamaica. Nature 343:417CrossRefGoogle Scholar
  23. Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley M, Baumann J, Matsui Y (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob Chang Biol 20:3823–3833CrossRefPubMedGoogle Scholar
  24. Guest JR, Baird AH, Maynard JA, Muttaqin E, Edwards AJ, Campbell SJ, Yewdall K, Affendi YA, Chou LM (2012) Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS One 7:e33353PubMedCentralCrossRefPubMedGoogle Scholar
  25. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322PubMedCentralCrossRefPubMedGoogle Scholar
  26. Hawkins TD, Davy SK (2012) Nitric oxide production and tolerance differ among Symbiodinium types exposed to heat stress. Plant Cell Physiol 53:1889–1898CrossRefPubMedGoogle Scholar
  27. Hawkins TD, Davy SK (2013) Nitric oxide and coral bleaching: is peroxynitrite generation required for symbiosis collapse? J Exp Biol 216:3185–3188CrossRefPubMedGoogle Scholar
  28. Hawkins TD, Krueger TK, Becker S, Fisher PL, Davy SK (2014) Differential nitric oxide synthesis and host apoptotic events correlate with bleaching susceptibility in reef corals. Coral Reefs 33:141–153CrossRefGoogle Scholar
  29. Jones RJ (2008) Coral bleaching, bleaching-induced mortality, and the adaptive significance of the bleaching response. Mar Biol 154:65–80CrossRefGoogle Scholar
  30. 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 21:1219–1230CrossRefGoogle Scholar
  31. Kenkel CD, Goodbody-Gringley G, Caillaud D, Davies SW, Bartels E, Matz MV (2013) Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments. Mol Ecol 22:4335–4348CrossRefPubMedGoogle Scholar
  32. Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346CrossRefPubMedGoogle Scholar
  33. Krueger T, Becker S, Pontasch S, Dove S, Hoegh-Guldberg O, Leggat W, Fisher PL, Davy SK (2014) Antioxidant plasticity and thermal sensitivity in four types of Symbiodinium sp. J Phycol 50:1035–1047CrossRefGoogle Scholar
  34. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400CrossRefGoogle Scholar
  35. Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41:271–283CrossRefGoogle Scholar
  36. Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192CrossRefGoogle Scholar
  37. Lesser MP (2006) Oxidative stress in marine environments. Annu Rev Physiol 68:253–278CrossRefPubMedGoogle Scholar
  38. Lesser MP (2011) Coral bleaching: causes and mechanisms. In: Dubinsky TJ, Stamler JS (eds) Coral reefs: an ecosystem in transition. Springer, Berlin, pp 405–419CrossRefGoogle Scholar
  39. Lesser MP, Shick JM (1989) Photoadaption and defenses against oxygen-toxicity in zooxanthellae from natural-populations of symbiotic cnidarians. J Exp Mar Biol Ecol 134:129–141CrossRefGoogle Scholar
  40. Lesser MP, Farrell JH (2004) Exposure to solar radiation increases damage to both host tissues and algal symbionts of corals during thermal stress. Coral Reefs 23:367–377CrossRefGoogle Scholar
  41. Lesser MP, Stochaj WR, Tapley DW, Shick JM (1990) Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8:225–232CrossRefGoogle Scholar
  42. Levy O, Achituv Y, Yacobi YZ, Stambler N, Dubinsky Z (2006) The impact of spectral composition and light periodicity on the activity of two antioxidant enzymes (SOD and CAT) in the coral Favia favus. J Exp Mar Biol Ecol 328:35–46CrossRefGoogle Scholar
  43. McGinty ES, Pieczonka J, Mydlarz LD (2012) Variations in reactive oxygen release and antioxidant activity in multiple Symbiodinium types in response to elevated temperature. Microb Ecol 64:1000–1007CrossRefPubMedGoogle Scholar
  44. Muscatine L, Hand C (1958) Direct evidence for the transfer of materials from symbiotic algae to the tissues of a coelenterate. Proc Natl Acad Sci U S A 44:1259–1263PubMedCentralCrossRefPubMedGoogle Scholar
  45. Mydlarz LD, McGinty ES, Harvell CD (2010) What are the physiological and immunological responses of coral to climate warming and disease? J Exp Biol 213:934–945CrossRefPubMedGoogle Scholar
  46. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  47. Nii CM, Muscatine L (1997) Oxidative stress in the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943): contribution of the animal to superoxide ion production at elevated temperature. Biol Bull 192:444–456CrossRefGoogle Scholar
  48. Paxton CW, Davy SK, Weis VM (2013) Stress and death of host cells play a role in cnidarian bleaching. J Exp Biol 216:2813–2820CrossRefPubMedGoogle Scholar
  49. Pontasch S, Hill R, Deschaseaux E, Fisher P, Davy S, Scott A (2014) Photochemical efficiency and antioxidant capacity in relation to Symbiodinium genotype and host phenotype in a symbiotic cnidarian. Mar Ecol Prog Ser 516:195–208CrossRefGoogle Scholar
  50. Porra R, Thompson W, Kriedemann P (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394CrossRefGoogle Scholar
  51. Putnam HM, Stat M, Pochon X, Gates RD (2012) Endosymbiotic flexibility associates with environmental sensitivity in scleractinian corals. Proc R Soc Lond B Biol Sci 279:4352–4361CrossRefGoogle Scholar
  52. Radi R, Peluffo G, Alvarez MN, Naviliat M, Cayota A (2001) Unraveling peroxynitrite formation in biological systems. Free Radic Biol Med 30:463–488CrossRefPubMedGoogle Scholar
  53. Reynolds JM, Bruns BU, Fitt WK, Schmidt GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci U S A 105:13674–13678PubMedCentralCrossRefPubMedGoogle Scholar
  54. Richier S, Furla P, Plantivaux A, Merle PL, Allemand D (2005) Symbiosis-induced adaptation to oxidative stress. J Exp Biol 208:277–285CrossRefPubMedGoogle Scholar
  55. Richier S, Sabourault C, Courtiade J, Zucchini N, Allemand D, Furla P (2006) Oxidative stress and apoptotic events during thermal stress in the symbiotic sea anemone, Anemonia viridis. FEBS J 273:4186–4198CrossRefPubMedGoogle Scholar
  56. Richier S, Cottalorda J-M, Guillarme MMM, Fernandez C, Allemand D, Furla P (2008) Depth-dependent response to light of the reef building coral, Pocillopora verrucosa: implication of oxidative stress. J Exp Mar Biol Ecol 357:48–56CrossRefGoogle Scholar
  57. Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci U S A 105:10444–10449PubMedCentralCrossRefPubMedGoogle Scholar
  58. Saragosti E, Tchernov D, Katsir A, Shaked Y (2010) Extracellular production and degradation of superoxide in the coral Stylophora pistillata and cultured Symbiodinium. PLoS One 5:e12508PubMedCentralCrossRefPubMedGoogle Scholar
  59. Shick JM, Lesser MP, Dunlap WC, Stochaj WR, Chalker BE, Won JW (1995) Depth-dependent responses to solar ultraviolet radiation and oxidative stress in the zooxanthellate coral Acropora microphthalma. Mar Biol 122:41–51CrossRefGoogle Scholar
  60. Silverstein RN, Cunning R, Baker AC (2014) Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob Chang Bio. 21:236–249CrossRefGoogle Scholar
  61. Stat M, Pochon X, Cowie ROM, Gates RD (2009) Specificity in communities of Symbiodinium in corals from Johnston Atoll. Mar Ecol Prog Ser 386:83–96CrossRefGoogle Scholar
  62. Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S, Baker NR (2008) Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J Phycol 44:948–956CrossRefGoogle Scholar
  63. Tchernov D, Kvitt H, Haramaty L, Bibby TS, Gorbunov MY, Rosenfeld H, Falkowski PG (2011) Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proc Natl Acad Sci U S A 108:9905–9909PubMedCentralCrossRefPubMedGoogle Scholar
  64. Tolleter D, Seneca F, DeNofrio J, Krediet C, Palumbi S, Pringle J, Grossman A (2013) Coral bleaching independent of photosynthetic activity. Curr Biol 23:1782–1786CrossRefPubMedGoogle Scholar
  65. Traylor-Knowles N, Palumbi SR (2014) Translational environmental biology: cell biology informing conservation. Trends Cell Biol 24:265–267CrossRefPubMedGoogle Scholar
  66. Veal CJ, Holmes G, Nunes M, Hoegh-Guldberg O, Osborne J (2010) A comparative study of methods for surface area and three dimensional shape measurement of coral skeletons. Limnol Oceanogr Methods 8:241–253Google Scholar
  67. Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci U S A 96:8007–8012PubMedCentralCrossRefPubMedGoogle Scholar
  68. Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066CrossRefPubMedGoogle Scholar
  69. Winterbourn CC (2008) Reconciling the chemistry and biology of reactive oxygen species. Nat Chem Biol 4:278–286CrossRefPubMedGoogle Scholar
  70. Yakovleva I, Bhagooli R, Takemura A, Hidaka M (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine. Comp Biochem Physiol B Biochem Mol Biol 139:721–730CrossRefPubMedGoogle Scholar
  71. Yakovleva IM, Baird AH, Yamamoto HH, Bhagooli R, Nonaka M, Hidaka M (2009) Algal symbionts increase oxidative damage and death in coral larvae at high temperatures. Mar Ecol Prog Ser 378:105–112CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Thomas D. Hawkins
    • 1
    • 2
  • Thomas Krueger
    • 1
    • 3
  • Shaun P. Wilkinson
    • 1
  • Paul L. Fisher
    • 1
    • 4
  • Simon K. Davy
    • 1
  1. 1.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand
  2. 2.College of Earth, Ocean and EnvironmentUniversity of DelawareLewesUSA
  3. 3.Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering (ENAC)École Polytechnique Fédérale de Lausanne (EPFL)LausanneSwitzerland
  4. 4.School of Civil EngineeringUniversity of QueenslandBrisbaneAustralia

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