Abstract
Coral bleaching (the loss of symbiotic dinoflagellates from reef-building corals) is most frequently caused by high-light and temperature conditions. We exposed the explants of the hermatypic coral Stylophora pistillata to four combinations of light and temperature in late spring and also in late summer. During mid-summer, two NOAA bleaching warnings were issued for Heron Island reef (Southern Great Barrier Reef, Australia) when sea temperature exceeded the NOAA bleaching threshold, and a ‘mild’ (in terms of the whole coral community) bleaching event occurred, resulting in widespread S. pistillata bleaching and mortality. Symbiotic dinoflagellate biomass decreased by more than half from late spring to late summer (from 2.5×106 to 0.8×106 dinoflagellates cm2 coral tissue), and those dinoflagellates that remained after summer became photoinhibited more readily (dark-adapted F V : F M decreased to (0.3 compared with 0.4 in spring), and died in greater numbers (up to 17% dinoflagellate mortality compared with 5% in the spring) when exposed to artificially elevated light and temperature. Adding exogenous antioxidants (d-mannitol and l-ascorbic acid) to the water surrounding the coral had no clear effect on either photoinhibition or symbiont mortality. These data show that light and temperature stress cause mortality of the dinoflagellate symbionts within the coral, and that susceptibility to light and temperature stress is strongly related to coral condition. Photoinhibitory mechanisms are clearly involved, and will increase through a positive feedback mechanism: symbiont loss promotes further symbiont loss as the light microenvironment becomes progressively harsher.
Similar content being viewed by others
References
Bethke PC, Lonsdale JE, Fath A, Jones RL (1999) Hormonally regulated programmed cell death in barley aleurone cells. Plant Cell 11:1033–1045
Bhagooli R, Hidaka M (2004) Release of zooxanthellae with intact photosynthetic activity by the coral Galaxea fascicularis in response to high temperature stress. Mar Biol 145:329–337
Brown BE, Le Tissier MDA, Bythell JC (1995) Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Mar Biol 122:655–663
Brussaard CPD, Marie D, Thyrhaug R, Bratbak G (2001) Flow cytometric analysis of phytoplankton viability following viral infection. Aquat Microb Ecol 26:157–166
Dunn SR, Bythell JC, Le Tissier MDA, Burnett WJ, Thomason JC (2002) Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the sea anemone Aiptasia sp. J Exp Mar Biol Ecol 272:29–53
Enríquez S, Méndez ER, Iglesias-Prieto R (2005) Multiple scattering by coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032
Fagoonee I, Wilson HB, Hassell MP, Turner JR (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843–845
Falkowski PG, Dubinsky Z, Muscatine L, McCloskey L (1993) Population control in symbiotic corals. BioScience 43:606–611
Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685
Fowler J, Cohen L (1995) Practical statistics for field biology. Wiley, Chichester, UK
Franklin LA, Levavasseur G, Osmond CB, Henley WJ, Ramus J (1992) Two components of onset and recovery during photoinhibition of Ulva rotundata. Planta 186:399–408
Franklin DJ, Hoegh-Guldberg O, Jones RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar Ecol Prog Ser 272:117–130
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
Gates RD, Muscatine L (1992) Three methods for isolating viable anthozoan endoderm cells with their intracellular symbiotic dinoflagellates. Coral Reefs 11:143–145
Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine. Clarendon press, Oxford
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
Jones RJ, Yellowlees D (1997) Regulation and control of intracellular algae (=zooxanthellae) in hard corals. Phil Trans R Soc Lond B 352:457–468
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
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 24:89–99
Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plant 74:566–574
LaJeunesse TC, Loh WKW, Van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK (2003) Low symbiont diversity in southern Great Barrier Reef corals, relative to those of the Caribbean. Limnol Oceanogr 48:2046–2054
Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192
Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:655–662
Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359
Ralph PJ, Gademann R, Larkum AWD (2001) Zooxanthellae expelled from bleached corals at 33°C are photosynthetically competent. Mar Ecol Prog Ser 220:163–168
Ralph PJ, Larkum AWD, Kühl M (2005) Temporal patterns in effective quantum yield of individual zooxanthellae expelled during bleaching. J Exp Mar Biol Ecol 316:17–28
Rees TAV (1991) Are symbiotic algae nutrient deficient? Proc R Soc Lond B 243:227–233
Smith GJ, Muscatine L (1999) Cell cycle of symbiotic dinoflagellates: variation in G1 phase-duration with anemone nutritional status and macronutrient supply in the Aiptasia pulchella-Symbiodinium pulchrorum symbiosis. Mar Biol 134:405–418
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
Stimson J (1997) The annual cycle of density of zooxanthellae in the tissues of field and laboratory-held Pocillopora damicornis (Linnaeus). J Exp Mar Biol Ecol 214:35–48
Takahashi S, Nakamura T, Sakamizu M, Van Woesik R, Yamasaki H (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol 45(2):251–255
Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Haggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Nat Acad Sci USA 101(37):13531–13535
Trench RK (1974) Nutritional potentials in Zoanthus sociathus (Coelenterata, Anthozoa). Helgolander wiss Meeresunters 26:174–216
Vardi A, Berman-Frank I, Rozenberg T, Hadas O, Kaplan A, Levine A (1999) Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO2 limitation and oxidative stress. Curr Biol 9:1061–1064
Veldhuis MJW, Kraay GW, Timmermans KR (2001) Cell death in marine phytoplankton: correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth. Eur J Phycol 36:167–177
Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012
Warner ME, Chilcoat GC, McFarland FK, Fitt WK (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastrea. Mar Biol 141:31–38
Wilkerson FP, Muller-Parker G, Muscatine L (1983) Temporal patterns of cell division in natural populations of endosymbiotic algae. Limnol Oceanogr 28:1009–1014
Acknowledgements
This work was funded by a Royal Society of London Fellowship to DJF and Australian Research Council funds (DP0453361) awarded to OHG. The work was also supported by the Global Environment Facility through the coral-reef-targeted research programme. We thank the students and staff of the Heron Island Research Station and the Centre for Marine Studies for assisting in the completion of this research.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Kühl, Helsingør
Rights and permissions
About this article
Cite this article
Franklin, D.J., Cedrés, C.M.M. & Hoegh-Guldberg, O. Increased mortality and photoinhibition in the symbiotic dinoflagellates of the Indo–Pacific coral Stylophora pistillata (Esper) after summer bleaching. Mar Biol 149, 633–642 (2006). https://doi.org/10.1007/s00227-005-0230-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-005-0230-z