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Metabolic plasticity of the corals Porites lutea and Diploastrea heliopora exposed to large amplitude internal waves

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Abstract

The metabolic plasticity of the two mounding coral species Porites lutea (Milne-Edwards and Haime, 1860) and Diploastrea heliopora (Lamarck, 1816) was investigated in the Similan Islands (Thailand), an offshore Andaman Sea island group subjected to large amplitude internal waves (LAIW). Nutrient concentrations were highly correlated with LAIW intensity and contributed to 3- and 10-fold higher symbiont densities in P. lutea and D. heliopora, respectively, along with elevated pigment concentrations, protein content, host tissue, and symbiont biomass. The comparison of LAIW-exposed and LAIW-sheltered island faces, and LAIW-intense and LAIW-weak years suggests a species-specific metabolic plasticity to LAIW, where D. heliopora benefits more from increased nutrient and organic matter availability than P. lutea. The ubiquitous LAIW in Southeast Asia and beyond may provide so far unexplored clues to coral acclimatization to disturbances on various scales, and hence, a potential key to coral resilience to climate change.

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References

  • Andrews JC, Gentien P (1982) Upwelling as a source of nutrients for the Great Barrier Reef ecosystems: a solution to Darwin’s question? Mar Ecol Prog Ser 8:257–269

    Article  Google Scholar 

  • Anthony KR, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253

    Article  PubMed  Google Scholar 

  • Anthony KR, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23:539–550

    Google Scholar 

  • Bachar A, Achituv Y, Pasternak Z, Dubinsky Z (2007) Autotrophy versus heterotrophy: the origin of carbon determines its fate in a symbiotic sea anemone. J Exp Mar Biol Ecol 349:295–298

    Article  CAS  Google Scholar 

  • Bagnato S, Linsley BK, Howe SS, Wellington GM, Salinger J (2004) Evaluating the use of the massive coral Diploastrea heliopora for paleoclimate reconstruction. Paleoceanography 19. doi:10.1029/2003PA000935

  • Bogucki D, Dickey T, Redekopp LG (1997) Sediment resuspension and mixing by resonantly generated internal solitary waves. J Phys Oceanogr 27:1181–1196

    Article  Google Scholar 

  • Brown BE (1997a) Coral bleaching: causes and consequences. Coral Reefs 16:129–138

    Article  Google Scholar 

  • Brown BE (1997b) Acclimatization of reef corals to physical environmental stress. Adv Mar Biol 31:221–299

    Article  Google Scholar 

  • Brown BE, Dunne RP, Ambarsari I, LeTissier MDA, Satapoomin S (1999) Seasonal fluctuations in environmental factors and variations in symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species. Mar Ecol Prog Ser 191:53–69

    Article  Google Scholar 

  • Buddemeier RW, Smith S (1999) Coral adaptation and acclimatization: a most ingenious paradox. Am Zool 39:1–9

    Google Scholar 

  • Capone DG, Carpenter EJ (1982) Nitrogen fixation in the marine environment. Science 217:1140–1142

    Article  PubMed  CAS  Google Scholar 

  • Chansang H, Satapoomin U, Poovachiranon S (1999) Maps of coral reefs in Thai waters, Andaman Sea. Coral Reef Resource Management Project, Department of Fisheries, Bangkok

    Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Zool 18:117–143

    Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Coles SL, Brown BE (2003) Coral bleaching-capacity for acclimatization and adaptation. Adv Mar Biol 46:183–223

    Article  PubMed  CAS  Google Scholar 

  • Corrège T, Gagan MK, Beck JW, Burr GS, Cabioch G, LeCornec F (2004) Interdecadal variation in the extent of South Pacific tropical waters during the Younger Dryas event. Nature 428:927–929

    Article  PubMed  Google Scholar 

  • Cortés J (1993) A reef under siltation stress: a decade of degradation. In: Ginsburg RN (ed) Colloquium on Global aspects of coral reefs: health, hazard and history. Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami

    Google Scholar 

  • Cortés J (1997) Biology and geology of eastern Pacific coral reefs. Coral Reefs 16(Suppl.):S39–S46

    Google Scholar 

  • Cortés-Núñez J, Risk MJ (1985) A reef under siltation stress: Cahuita, Costa Rica. Bull Mar Sci 36:339–356

    Google Scholar 

  • de Goeij JM, van Duyl FC (2007) Coral cavities are sinks of dissolved organic carbon (DOC). Limnol Oceanogr 52:2608–2617

    Article  Google Scholar 

  • Dickson M-L, Wheeler PA (1995) Ammonium uptake and regeneration rates in a coastal upwelling regime. Mar Ecol Prog Ser 121:239–248

    Article  CAS  Google Scholar 

  • Dixon WJ, Mood AM (1946) The statistical sign test. J Am Statist Assoc 41:557–566

    Article  CAS  Google Scholar 

  • Dollar SJ (1982) Wave stress and coral community structure in Hawaii. Coral Reefs 1:71–81

    Article  Google Scholar 

  • Dollar SJ, Tribble GW (1993) Recurrent storm disturbance and recovery: a long-term study of coral communities in Hawaii. Coral Reefs 12:223–233

    Article  Google Scholar 

  • Done T (1992) Constancy and change in some Great Barrier Reef coral communities: 1980–1990. Am Zool 32:655–662

    Google Scholar 

  • Dortch Q (1990) The interaction between ammonium and nitrate uptake in phytoplankton. Mar Ecol Prog Ser 61:183–201

    Article  CAS  Google Scholar 

  • Dunne RP, Brown BE (1996) Penetration of solar UVB radiation in shallow tropical waters and its potential biological effects on coral reefs; results from the central Indian Ocean and Andaman Sea. Mar Ecol Prog Ser 144:109–118

    Article  Google Scholar 

  • Edinger E, Limmon GV, Jompa J, Widjatmoko W, Heikoop JM, Risk MJ (2000) Normal coral growth rates on dying reefs: are coral growth rates good indicators of reef health? Mar Pollut Bull 40:404–425

    Article  CAS  Google Scholar 

  • Enríquez S, Méndez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032

    Article  Google Scholar 

  • Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146

    Article  PubMed  CAS  Google Scholar 

  • Fagoonee I, Wilson HB, Hassell MB, Turner JR (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843–845

    Article  PubMed  CAS  Google Scholar 

  • Feely RA, Sabine CL, Hernandez-Ayon M, Ianson D, Hales B (2008) Evidence for upwelling of corrosive “acidified” water onto the continental shelf. Science 320:1490–1492

    Article  PubMed  CAS  Google Scholar 

  • Fine M, Tchernov D (2007) Scleractinian coral species survive and recover from decalcification. Science 315:1811

    Article  PubMed  CAS  Google Scholar 

  • Fitt W, McFarland F, Warner M, Chilcoat G (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685

    Article  CAS  Google Scholar 

  • Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43

    Google Scholar 

  • Gleason MG (1993) Effects of disturbance on coral reef communities: bleaching in Morea, French Polynesia. Coral Reefs 12:193–201

    Article  Google Scholar 

  • Glynn P (1990) Coral mortality and disturbances to coral reefs in the tropical eastern Pacific. In: Glynn P (ed) Global ecological consequences of the 1982–83 El Nino-Southern Oscillation. Elsevier, Amsterdam

    Google Scholar 

  • Gonzalez L, Manly BFJ (1998) Analysis of variance by randomization with small data sets. Environmetrics 9:53–65

    Article  Google Scholar 

  • Grasshof K (1983) Methods of seawater analysis, 2nd edn. Verlag Chemie, Weinheim

    Google Scholar 

  • Grigg RW (1998) Holocene coral reef accretion in Hawaii: a function of wave exposure and sea level history. Coral Reefs 17:263–272

    Article  Google Scholar 

  • Grimsditch G, Mwaura J, Kilonzo J, Amiyo N, Obdura D (2008) Zooxanthellae densities are highest in summer months in equatorial corals in Kenya. In: Obdura D, Tamelander J, Linden O (eds) Ten years after bleaching—facing the consequences of climate change in the Indian Ocean CORIDO Status Report 2008. Coastal Ocean Research and Development in the Indian Ocean/Sida-SAREC, Mombasa

    Google Scholar 

  • Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol 145:621–631

    Article  CAS  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189

    Article  PubMed  CAS  Google Scholar 

  • Harriott VJ (1985) Mortality rates of scleractinian corals before and during a mass bleaching event. Mar Ecol Prog Ser 21:81–88

    Article  Google Scholar 

  • Hearn C, Atkinson M, Falter J (2001) A physical derivation of nutrient-uptake rates in coral reefs: effects of roughness and waves. Coral Reefs 20:347–356

    Article  Google Scholar 

  • Heikoop JM, Risk MJ, Lazier AV, Edinger EE, Jompa J, Limmon GV, Dunn JJ, Browne DR, Schwarcz HP (2000) Nitrogen-15 signals of anthropogenic nutrient loading in reef corals. Mar Pollut Bull 40:628–636

    Article  CAS  Google Scholar 

  • Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Article  Google Scholar 

  • Hoegh-Guldberg O, Smith GJ (1989a) The effect of sudden changes in temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana. J Exp Mar Biol Ecol 129:279–303

    Article  Google Scholar 

  • Hoegh-Guldberg O, Smith J (1989b) Influence of the population density of zooxanthellae and supply of ammonium on the biomass and metabolic characteristics of the reef corals Seriatopora hystrix and Stylophora pistillata. Mar Ecol Prog Ser 57:173–186

    Article  CAS  Google Scholar 

  • Hughes T, Baird A, Bellwood D, Card M, Connolly AR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson J, Kleypas J, Lough J, Marshall P, Nyström M, Palumbi S, Pandolfi J, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  PubMed  CAS  Google Scholar 

  • Jackson CR (2004) An atlas of internal solitary-like waves and their properties. Global Ocean Association 2nd edition

  • Kattner G (1999) Storage of dissolved inorganic nutrients in seawater: poisoning with mercury chloride. Mar Chem 67:61–66

    Article  CAS  Google Scholar 

  • Kinsey DW (1988) Coral reef system response to some natural and anthropogenic stresses. Galaxea 7:113–128

    Google Scholar 

  • Kinsey DW, Davies PJ (1979) Effects of elevated nitrogen and phosphorus on coral reef growth. Limnol Oceanogr 24:935–940

    Article  CAS  Google Scholar 

  • Kokkinakis SA, Wheeler PA (1987) Nitrogen uptake and phytoplankton growth in coastal upwelling regions. Limnol Oceanogr 32:1112–1123

    Article  CAS  Google Scholar 

  • Lapointe BE (1997) Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and south Florida. Limnol Oceanogr 42:1119–1131

    Article  CAS  Google Scholar 

  • Larned S (1998) Nitrogen- versus phosphorus-limited growth and sources of nutrients for coral reef macroalgae. Mar Biol 132:409–421

    Article  Google Scholar 

  • Leichter JJ, Genovese SJ (2006) Intermittent upwelling and subsidized growth of the scleractinian coral Madracis mirabilis on the deep fore-reef slope of Discovery Bay, Jamaica. Mar Ecol Prog Ser 316:95–103

    Article  Google Scholar 

  • Leichter JJ, Shellenbarger G, Genovese SJ, Wing SR (1998) Breaking internal waves on a Florida (USA) coral reef: a plankton pump at work? Mar Ecol Prog Ser 166:83–97

    Article  Google Scholar 

  • Leichter JJ, Stewart HL, Miller SL (2003) Episodic nutrient transport to Florida coral reefs. Limnol Oceanogr 48:1394–1407

    Article  Google Scholar 

  • Lewis JB (1977) Processes of organic production on coral reefs. Biol Rev 52:305–347

    Article  CAS  Google Scholar 

  • Lorenzen CJ (1967) Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol Oceanogr 12:343–346

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Muscatine L, D’Elia C (1978) The uptake, retention, and release of ammonium by reef corals. Limnol Oceanogr 23:725–734

    Article  CAS  Google Scholar 

  • Muscatine L, Porter JW (1977) Reef corals: Mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460

    Article  Google Scholar 

  • Muscatine L, Porter JW, Kaplan IR (1989a) Resource partitioning by reef corals as determined from stable isotope composition. Mar Biol 100:185–193

    Article  Google Scholar 

  • Muscatine L, Falkowski PG, Dubinsky Z, Cook PA, McCloskey LR (1989b) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proc R Entomol Soc Lond 236:311–324

    Article  Google Scholar 

  • Naumann M, Niggl W, Laforsch C, Glaser C, Wild C (2009) Coral surface area quantification–evaluation of established techniques by comparison with computer tomography. Coral Reefs 28:109–117

    Article  Google Scholar 

  • Oku H, Yamashiro H, Onaga K, Sakai K, Iwasaki H (2003) Seasonal changes in the content and composition of lipids in the coral Goniastrea aspera. Coral Reefs 22:83–85

    Google Scholar 

  • Osborne AR, Burch TI (1980) Internal solitons in the Andaman Sea. Science 208:451–460

    Article  PubMed  CAS  Google Scholar 

  • Palardy JE, Grottoli AG, Matthews KA (2005) Effects of upwelling, depth, morphology and polyp size on feeding in three species of Panamanian corals. Mar Ecol Prog Ser 300:79–89

    Article  Google Scholar 

  • Pineda J (1999) Circulation and larval distribution in internal tidal bore warm fronts. Limnol Oceanogr 44:1400–1414

    Article  Google Scholar 

  • Porter JW (1976) Autotrophy, heterotrophy, and resource partitioning in Caribbean reef-building corals. Am Nat 110:731–742

    Article  Google Scholar 

  • Roder C, Fillinger L, Jantzen C, Schmidt GM, Khokiattiwong S, Richter C (2010) Trophic response of corals to large amplitude internal waves. Mar Ecol Prog Ser 412:113–128

    Article  CAS  Google Scholar 

  • Rodrigues LJ, Grottoli AG (2006) Calcification rate and the stable carbon, oxygen, and nitrogen isotopes in the skeleton, host tissue, and zooxanthellae of bleached and recovering Hawaiian corals. Geochim Cosmochim Acta 70:2781–2789

    Article  CAS  Google Scholar 

  • Sawall Y, Phongsuwan N, Richter C (2010) Coral recruitment and recovery after the 2004 Tsunami around the Phi Phi Islands (Krabi Province) and Phuket, Andaman Sea, Thailand. Helgol Mar Res 64:357–365

    Google Scholar 

  • Schmidt G (2010) Corals and waves: Calcification and bioerosion in large amplitude internal wave (LAIW) affected coral reefs. PhD dissertation, Bremen University, p 193

  • Sebens KP, DeRiemer K (1977) Diel cycles of expansion and contraction in coral reef anthozoans. Mar Biol 43:247–256

    Article  Google Scholar 

  • Shashar N, Cohen Y, Loya Y (1993) Extreme diel fluxes of oxygen in diffusive boundary layers surrounding stony corals. Biol Bull 185:455–461

    Article  Google Scholar 

  • Sheppard C (2009) Large temperature plunges recorded by data loggers at different depths on an Indian Ocean atoll: comparison with satellite data and relevance to coral refuges. Coral Reefs 28:399–403

    Article  Google Scholar 

  • Stanley GD (2003) The evolution of modern corals and their early history. Earth Sci Rev 60:195–225

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Stimson J, Sakai K, Sembali H (2002) Interspecific comparison of the symbiotic relationship in corals with high and low rates of bleaching-induced mortality. Coral Reefs 21:409–421

    Google Scholar 

  • Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Bull Fish Res Board Can 167

  • Sunagawa S, Cortés J, Jimenez C, Lara R (2008) Variation in cell densities and pigment concentrations of symbiotic dinoflagellates in the coral Pavona clavus in the eastern Pacific (Costa Rica). Cienc Mar 34:113–123

    Google Scholar 

  • Swart PK, Saied A, Lamb K (2005) Temporal and spatial variation in the δ15N and δ13C of coral tissue and zooxanthellae in Montastrea faveolata collected from the Florida reef tract. Limnol Oceanogr 50:1049–1058

    Article  CAS  Google Scholar 

  • Szmant A, Gassman NJ (1990) The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217–224

    Article  Google Scholar 

  • van Duyl FC, Gast GJ (2001) Linkage of small-scale spatial variations in DOC, inorganic nutrients and bacterioplankton growth with different coral reef water types. Aquat Microb Ecol 24:17–26

    Article  Google Scholar 

  • Veron JEN (1995) Corals in space and time: the biogeography and evolution of the scleractinia. Cornell University Press, Ithaca

    Google Scholar 

  • Veron JEN, Stafford-Smith M (2000) Corals of the world. Australian Institute of Marine Science

  • Vlasenko V, Alpers W (2005) Generation of secondary internal waves by the interaction of an internal solitary wave with an underwater bank. J Geophys Res 110. doi:10.1029/2004JC002467

  • Vlasenko V, Hutter K (2002) Numerical experiments on the breaking of solitary internal waves over a slope-shelf topography. J Phys Oceanogr 32:1779–1793

    Article  Google Scholar 

  • Vlasenko V, Stashchuk N (2007) Three-dimensional shoaling of large-amplitude internal waves. J Geophys Res 112. doi:10.1029/2007JC004107

  • Ward BB, Talbot MC, Perry MJ (1984) Contributions of phytoplankton and nitrifying bacteria to ammonium and nitrite dynamics in coastal waters. Cont Shelf Res 3:383–398

    Article  Google Scholar 

  • Watanabe T, Gagan MK, Corrège T, Scott-Gagan H, Cowley J, Hantoro WS (2003) Oxygen isotope systematics in Diploastrea heliopora: new coral archive of tropical paleoclimate. Geochim Cosmochim Acta 67:1349–1358

    Article  CAS  Google Scholar 

  • Wiebe W, Johannes R, Webb K (1975) Nitrogen fixation in a coral reef community. Science 188:257–259

    Article  PubMed  CAS  Google Scholar 

  • Wild C, Huettel M, Klueter A, Kremb S, Rasheed M, Jørgensen B (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70

    Article  PubMed  CAS  Google Scholar 

  • Witman JD, Leichter JJ, Genovese SJ, Brooks DA (1993) Pulsed phytoplankton supply to the rocky subtidal zone: Influence of internal waves. Proc Natl Acad Sci USA 90:1686–1690

    Article  PubMed  CAS  Google Scholar 

  • Wolanski E, Delesalle B (1995) Upwelling by internal waves, Tahiti, French Polynesia. Cont Shelf Res 15:357–368

    Article  Google Scholar 

  • Woodley JD (1992) The incidence of hurricanes on the north coast of Jamaica since 1870: are the classic reef descriptions atypical? Hydrobiologia 247:133–138

    Article  Google Scholar 

  • Wooldridge SA (2009) Water quality and coral bleaching thresholds: formalising the linkage for the inshore reefs of the Great Barrier Reef, Australia. Mar Pollut Bull 58:745–751

    Article  PubMed  CAS  Google Scholar 

  • Wooldridge SA, Done TJ (2009) Improved water quality can ameliorate effects of climate change on corals. Ecol Appl 19:1492–1499

    Article  PubMed  Google Scholar 

  • Wu G, Zhang Y (1998) Tibetan plateau forcing and the timing of the monsoon onset over South Asia and the South China Sea. Am Meteorol Soc 126:913–927

    Google Scholar 

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Acknowledgments

Research was funded by the German Research Foundation (DFG Förderkennzeichen RI 1074/7-1) and the National Research Council of Thailand (NRCT). The authors would like to thank the Phuket Marine Biological Center and the National Park Mu Koh Similan staff for field support, as well as Somkiat Khokiattiwong for coordination, and Dorothee Dasbach and Kai-Uwe Ludwichowski for laboratory assistance. We thank Dr. Clifford Hearn and three anonymous reviewers for useful comments and suggestions improving the manuscript.

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Roder, C., Jantzen, C., Schmidt, G.M. et al. Metabolic plasticity of the corals Porites lutea and Diploastrea heliopora exposed to large amplitude internal waves. Coral Reefs 30 (Suppl 1), 57–69 (2011). https://doi.org/10.1007/s00338-011-0722-x

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