Abstract
We examined quantitative changes in the metabolism of the coral Galaxea fascicularis caused by increases in both hydrogen peroxide (H2O2) concentration and seawater temperature. Seawater temperatures were maintained at 27 or 31°C in a well-controlled incubation chamber, and three levels of H2O2 concentration (0, 0.3, 3.0 μM) were used in experimental treatments. Gross primary production, calcification rates and respiration rates were all affected by increased H2O2 concentrations and high seawater temperatures. Individual treatments of high H2O2 or elevated seawater temperature alone caused significant declines in coral photosynthesis and calcification rates within the 3-day incubation period. The synergistic effect of high H2O2 combined with high seawater temperature resulted in a 134% increase in respiration rates, which surpassed the effect of either H2O2 or high seawater temperature alone. Our results suggest that both high H2O2 concentrations and elevated temperatures in seawater can strongly affect coral metabolism; however, these effects cannot be estimated by simply summing the effects of individual stress parameters.
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Al-Horani FA, Tambutté É, Allemand D (2007) Dark calcification and the daily rhythm of calcification in the scleractinian coral, Galaxea fascicularis. Coral Reefs 26:531–538. doi:https://doi.org/10.1007/s00338-007-0250-x
Arakaki T, Fujimura H, Hamdun AM, Okada K, Kondo H, Oomori T, Tanahara A, Taira H (2005) Simultaneous measurement of hydrogen peroxide and Fe species (Fe(II) and Fe(tot)) in Okinawa island seawater: impact of red soil pollution. J Oceanogr 61:561–568. doi:https://doi.org/10.1007/s10872-005-0064-9
Arakaki T, Ikota H, Okada K, Kuroki Y, Nakajima H, Tanahara A (2007) Behavior of hydrogen peroxide between atmosphere and coastal seawater around Okinawa Island. Chikyukagaku Geochem 41:35–41
Avery GB, Cooper WJ, Kieber RJ, Willey JD (2005) Hydrogen peroxide at the Bermuda Atlantic Time Series Station: temporal variability of seawater hydrogen peroxide. Mar Chem 97(3–4):236–244. doi:https://doi.org/10.1016/j.marchem.2005.03.006
Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:129–138. doi:https://doi.org/10.1007/s003380050249
Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol (Berl) 43:209–216. doi:https://doi.org/10.1007/BF00402313
Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 33(4):533–543. doi:https://doi.org/10.1016/S0891-5849(02)00907-3
Dykens JA, Shick JM (1982) Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297:579–580. doi:https://doi.org/10.1038/297579a0
Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50(2):125–146. doi:https://doi.org/10.1016/j.marpolbul.2004.11.028
Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65. doi:https://doi.org/10.1007/s003380100146
Fridovich I (1986) Biological effects of the superoxide radical. Arch Biochem Biophys 247:1–11. doi:https://doi.org/10.1016/0003-9861(86)90526-6
Fujimura H, Oomori T, Maehira T, Miyahira K (2001) Changes of coral carbon metabolism influenced by coral bleaching. Galaxea JCRS 3:41–50
Fujimura H, Higuchi T, Shiroma K, Arakaki T, Hamdun AM, Nakano Y, Oomori T (2008) Continuous-flow complete-mixing system for assessing the effects of environmental factors on colony-level coral metabolism. Biochem Biophys Methods 70:865–872. doi:https://doi.org/10.1016/j.jprot.2008.01.014
Hayashibara T, Iwao K, Omori M (2004) Induction and control of spawning in Okinawan staghorn corals. Coral Reefs 23:406–409. doi:https://doi.org/10.1007/s00338-004-0406-x
Jahnke LS, White AL (2003) Long-term hyposaline and hypersaline stresses produce distinct antioxidant responses in the marine alga Dunaliella tertiolecta. J Plant Physiol 160:1193–1202. doi:https://doi.org/10.1078/0176-1617-01068
Kinsey DW (1983) Standards of performance in coral reef primary production and carbon turnover. In: Barnes DJ (ed) Perspectives on coral reefs. Australian Institute of Marine Science by Brian Clouston Publisher, Australia, pp 209–219
Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192. doi:https://doi.org/10.1007/s003380050073
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 8:225–232. doi:https://doi.org/10.1007/BF00265015
Lesser MP, Weis VM, Patterson MR, Jokiel PL (1994) Effects of morphology and water motion on carbon delivery and productivity in the reef coral, Pocillopora damicornis (Linnaeus): diffusion barriers, inorganic carbon limitation, and biochemical plasticity. J Exp Mar Biol Ecol 178:153–179. doi:https://doi.org/10.1016/0022-0981(94)90034-5
Levy O, Achituv Y, Yacoci 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 328:35–46. doi:https://doi.org/10.1016/j.jembe.2005.06.018
Miller WL, Kester DR (1988) Hydrogen peroxide measurement in seawater by (p-hydroxyphenyl)acetic acid dimerization. Anal Chem 60:2711–2715. doi:https://doi.org/10.1021/ac00175a014
Nakajima H, Okada K, Fujimura H, Arakaki T, Tanahara A (2004) Photochemical formation of peroxides in coastal seawater around Okinawa Island. Bunseki Kagaku 53(9):891–897. doi:https://doi.org/10.2116/bunsekikagaku.53.891 (in Japanese with English abstract)
Nyström M, Nordemar I, Tedengren M (2001) Simultaneous and sequential stress from increased temperature and copper on the metabolism of hermatypic coral Porites cylindrica. Mar Biol (Berl) 138:1225–1231. doi:https://doi.org/10.1007/s002270100549
Nordemar I, Nyström M, Dizon R (2003) Effects of elevated seawater temperature and nitrate enrichment on the branching coral Porites cylindrical in the absence of particulate food. Mar Biol (Berl) 142:669–677
Omija T (2004) Terrestrial inflow of soils and nutrients. In: The Japanese Coral Reef Society and Ministry of the Environment (eds) Coral reefs of Japan. Ministry of the Environment, Tokyo, Japan, pp 64–68
Pires A, Hadfield MG (1991) Oxidative breakdown products of Catecholamines and hydrogen peroxide induce partial metamorphosis in the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthibranchia). Biol Bull 180:310–317. doi:https://doi.org/10.2307/1542402
Porter JW, Lewis SK, Porter KG (1999) The effect of multiple stressors on the Florida Keys coral reef ecosystem: a landscape hypothesis and a physiological test. Limnol Oceanogr 44:941–949
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 zooxanthellae coral Acropora microphthalma. Mar Biol (Berl) 122:41–51. doi:https://doi.org/10.1007/BF00349276
Smith SV, Key GS (1975) Carbon dioxide and metabolism in marine environments. Limnol Oceanogr 20:493–495
Yakovleva I, Bhagooli R, Takemura A, Hidaka M (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glicine. Comp Biochem Physiol B 139:721–730
Zika R, Saltzaman E, Chameides WL, Davis DD (1982) H2O2 levels in rain water collected in South Florida and the Bahama islands. J Geophys Res 87:5015–5017. doi:https://doi.org/10.1029/JC087iC07p05015
Acknowledgments
We thank Dr. H. Wang of the University of Maryland University College, Okinawa, for valuable comments on the manuscript. This study was supported by a Grant-in-Aid for Scientific Research (C) from the Japan Society for the Promotion of Science (no. 17510013) and by the 21st Century COE program of the University of the Ryukyus.
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Communicated by H. O. Pörtner.
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Higuchi, T., Fujimura, H., Arakaki, T. et al. The synergistic effects of hydrogen peroxide and elevated seawater temperature on the metabolic activity of the coral Galaxea fascicularis . Mar Biol 156, 589–596 (2009). https://doi.org/10.1007/s00227-008-1110-0
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DOI: https://doi.org/10.1007/s00227-008-1110-0