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Coral Reefs

, Volume 38, Issue 1, pp 149–163 | Cite as

The effect of warming and benthic community acclimation on coral reef carbonate sediment metabolism and dissolution

  • Coulson A. LantzEmail author
  • Kai G. Schulz
  • Bradley D. Eyre
Report

Abstract

Global warming (and the consequent increase in sea surface temperature) is expected to modify rates of gross primary production (GPP), respiration (R), and net calcium carbonate (CaCO3) dissolution in permeable coral reef carbonate sediments. Previous simulations of seawater warming on coral reef sediments found a decline in the GPP/R ratio and an associated increase in CaCO3 dissolution but were only conducted over a short timescale (< 24 h). To date, no studies have examined the prolonged (> 24 h) effect of seawater warming on coral reef CaCO3 sediment metabolism and dissolution, which may allow the benthic community to acclimatise. This study used 600-L flume aquaria to examine the effect of seawater warming on GPP, R, and CaCO3 dissolution in the permeable coral reef CaCO3 sediments of Mo’orea, French Polynesia, over a period of 15 d. On average, when exposed to warmed seawater (+ 2.8 °C), R in the CaCO3 sediments was enhanced (+ 58%) to a greater extent than GPP (+19%), resulting in a decline in GPP/R (− 23%) and an associated increase in net CaCO3 dissolution (+ 126%). The magnitude of these warming-mediated metabolic changes increased each day until reaching a plateau after about 8 d, indicating that 24-h experiments may be underestimating the effect of warming over longer timescales. Interestingly, the increase in dissolution relative to control treatments was more striking during the day (+ 163%) than at night (+ 89%), suggesting that warming acted to both enhance geochemical dissolution and reduce biogenic calcification or inorganic precipitation. Together, these data indicate that, over the timescale observed here, photosynthesis and associated inorganic and biogenic CaCO3 precipitation do not exhibit the ability to counterbalance the warming-mediated increase in sediment heterotrophy and CaCO3 dissolution.

Keywords

Dissolution Sediment Coral reef Global warming 

Notes

Acknowledgements

This research was conducted at the Richard B. Gump South Pacific Research Station (UC Berkeley) in collaboration with the Mo’orea Coral Reef Long-Term Ecological Research (MCR LTER) programme. We would like to thank Jesse Bergman-Lantz, Steve Doo, and Griffin Srednick for their assistance in the field. This research was funded by ARC Discovery Grant DP150102092 and the US National Science Foundation (OCE 14-15268 and 12-36905).

References

  1. Adey WH (1998) Coral reefs: Algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. J Phycol 34:393–406CrossRefGoogle Scholar
  2. Al-horani FA (2005) Effects of changing seawater temperature on photosynthesis and calcification in the scleractinian coral Galaxea fascicularis, measured with O2, Ca2+ and pH microsensors. Sci Mar 69:347–354CrossRefGoogle Scholar
  3. Andersson AJ (2015) A fundamental paradigm for coral reef carbonate sediment dissolution. Front Mar Sci 2:52CrossRefGoogle Scholar
  4. Ashton GV, Morley SA, Barnes DKA, Clark MS, Peck LS (2017) Warming by 1°C Drives Species and Assemblage Level Responses in Antarctica’s Marine Shallows. Curr Biol 27(17):2698–2705CrossRefGoogle Scholar
  5. Atkinson MJ (2011) Biogeochemistry of nutrients. Coral Reefs: An Ecosystem in Transition. Springer Netherlands, Dordrecht, pp 199–206Google Scholar
  6. Bahr KD, Jokiel PL, Rodgers KS (2016) Influence of solar irradiance on underwater temperature recorded by temperature loggers on coral reefs. Limnol Oceanogr Methods 14:n/a–n/aGoogle Scholar
  7. Barnes DJ, Chalker BE (1990) Calcification and photosynthesis in reef-building corals and algae. Ecosystems of the World: Coral Reefs. Elsevier, pp 109–131Google Scholar
  8. Chalker BE, Taylor DL (1975) Light-enhanced calcification, and the role of oxidative phosphorylation in calcification of the coral Acropora cervicornis. Proc R Soc London Ser B, Biol Sci 190:323–331Google Scholar
  9. Chanson M, Millero FJ (2007) Effect of filtration on the total alkalinity of open-ocean seawater. Limnol Oceanogr Methods 5:293–295CrossRefGoogle Scholar
  10. Clarke A (2003) Costs and consequences of evolutionary temperature adaptation. Trends Ecol Evol 18:573–581CrossRefGoogle Scholar
  11. Cohen A, Holcomb M (2009) Why corals care about ocean acidification: uncovering the mechanism. Oceanography 22:118–127CrossRefGoogle Scholar
  12. Comeau S, Carpenter RC, Lantz CA, Edmunds PJ (2015) Ocean acidification accelerates dissolution of experimental coral reef communities. Biogeosciences 12:365–372CrossRefGoogle Scholar
  13. Comeau S, Carpenter RC, Lantz CA, Edmunds PJ (2016) Parameterization of the response of calcification to temperature and pCO2in the coral Acropora pulchra and the alga Lithophyllum kotschyanum. Coral Reefs 35:929–939CrossRefGoogle Scholar
  14. Cyronak T, Santos IR, McMahon A, Eyre BD (2013) Carbon cycling hysteresis in permeable carbonate sands over a diel cycle: Implications for ocean acidification. Limnol Oceanogr 58:131–143CrossRefGoogle Scholar
  15. Cyronak T, Eyre BD (2016) The synergistic effects of ocean acidification and organic metabolism on calcium carbonate (CaCO3) dissolution in coral reef sediments. Mar Chem 183:1–12CrossRefGoogle Scholar
  16. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. North Pacific Marine Science OrganizationGoogle Scholar
  17. Eyre BD, Ferguson AJP, Webb A, Maher D, Oakes JM (2011) Metabolism of different benthic habitats and their contribution to the carbon budget of a shallow oligotrophic sub-tropical coastal system (southern Moreton Bay, Australia). Biogeochemistry 102:87–110CrossRefGoogle Scholar
  18. Eyre BD, Andersson AJ, Cyronak T (2014) Benthic coral reef calcium carbonate dissolution in an acidifying ocean. Nat Clim Chang 4:969–976CrossRefGoogle Scholar
  19. Eyre BD, Cyronak T, Drupp P, De Carlo EH, Sachs JP, Andersson AJ (2018) Coral reefs will transition to net dissolving before end of century. Science 359:908–911CrossRefGoogle Scholar
  20. Fofonoff NP, Millard Jr RC (1983) Algorithms for the computation of fundamental properties of seawater. Paris, France, UNESCO, 53 pp. (UNESCO Technical Papers in Marine Sciences; 44). https://www.hdl.handle.net/11329/109
  21. Frommlet JC, Sousa ML, Alves A, Vieira SI, Suggett DJ, Serôdio J (2015) Coral symbiotic algae calcify ex hospite in partnership with bacteria. Proc Natl Acad Sci 112:6158–6163CrossRefGoogle Scholar
  22. Gattuso JP, Pichon M, Delesalle B, Canon C, Frankignoulle M (1996) Carbon fluxes in coral reefs. I. Lagrangian measurement of community metabolism and resulting air-sea CO2 disequilibrium. Mar Ecol Prog Ser 145:109–121CrossRefGoogle Scholar
  23. Gattuso J-P, Magnan A, Billé R, Cheung WWL, Howes EL, Joos F, Allemand D (2015) Oceanography. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349:4722CrossRefGoogle Scholar
  24. Glud RN, Eyre BD, Patten N (2008) Biogeochemical responses to mass coral spawning at the Great Barrier Reef: Effects on respiration and primary production. Limnol Oceanogr 53:1014–1024CrossRefGoogle Scholar
  25. Hancke K, Sorrell BK, Chresten Lund-Hansen L, Larsen M, Hancke T, Glud RN (2014) Effects of temperature and irradiance on a benthic microalgae community: A combined two-dimensional oxygen and fluorescence imaging approach. Limnol Oceanogr 59:1599–1611CrossRefGoogle Scholar
  26. Hansen LA, Alongi DM, Moriarty DJW, Pollard PC (1987) The dynamics of benthic microbial communities at Davies Reef, central Great Barrier Reef. Coral Reefs 6:63–70CrossRefGoogle Scholar
  27. Harvey BP, Gwynn-Jones D, Moore PJ (2013) Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol Evol 3:1016–1030CrossRefGoogle Scholar
  28. Hewson I, Fuhrman JA (2006) Spatial and vertical biogeography of coral reef sediment bacterial and diazotroph communities. Mar Ecol Prog Ser 306:79–86CrossRefGoogle Scholar
  29. Holcomb M, Cohen AL, Gabitov RI, Hutter JL (2009) Compositional and morphological features of aragonite precipitated experimentally from seawater and biogenically by corals. Geochim Cosmochim Acta 73:4166–4179CrossRefGoogle Scholar
  30. Howe SA, Marshall AT (2002) Temperature effects on calcification rate and skeletal deposition in the temperate coral, Plesiastrea versipora (Lamarck). J Exp Mar Bio Ecol 275:63–81CrossRefGoogle Scholar
  31. IPCC Summary for policymakers. Climate Change (2013) The Physical Science Basis Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY USAGoogle Scholar
  32. Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochemical Physiology Pflanz 167: 191–194. Biochem Physiol Pflanz 191–194Google Scholar
  33. Jokiel PL, Coles SL (1977) Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar Biol 43:201–208CrossRefGoogle Scholar
  34. Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155–162CrossRefGoogle Scholar
  35. Jokiel PL (2013) Coral reef calcification: carbonate, bicarbonate and proton flux under conditions of increasing ocean acidification. Proceedings Biol Sci 280:20130031CrossRefGoogle Scholar
  36. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso J-P (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Chang Biol 19:1884–1896CrossRefGoogle Scholar
  37. Lantz CA, Schulz KG, Stoltenberg L, Eyre BD (2017) The short-term combined effects of temperature and organic matter enrichment on permeable coral reef carbonate sediment metabolism and dissolution. Biogeosciences 145194:5377–5391CrossRefGoogle Scholar
  38. Levitus S, Antonov JI, Boyer TP, Stephens C (2000) Warming of the World Ocean. Science (80-) 287:2225–2229CrossRefGoogle Scholar
  39. Littman RA, van Oppen MJH, Willis BL (2008) Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef). J Exp Mar Bio Ecol 364:48–53CrossRefGoogle Scholar
  40. Lohbeck KT, Riebesell U, Reusch TBH (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci 5:346–351CrossRefGoogle Scholar
  41. Marshall AT, Clode P (2004) Calcification rate and the effect of temperature in a zooxanthellate and an azooxanthellate scleractinian reef coral. Coral Reefs 23:218–224Google Scholar
  42. McNeil BI, Matear RJ, Barnes DJ (2004) Coral reef calcification and climate change: The effect of ocean warming. Geophys Res Lett 31Google Scholar
  43. Orlando JL, Yee SH (2016) Linking Terrigenous Sediment Delivery to Declines in Coral Reef Ecosystem Services. Estuaries and Coasts 40:1–17Google Scholar
  44. Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078CrossRefGoogle Scholar
  45. Revsbech NP, Jørgensen BB (1986) Microelectrodes: Their Use in Microbial Ecology. Springer, Boston, MA, pp 293–352Google Scholar
  46. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134CrossRefGoogle Scholar
  47. Santos IR, Eyre BD, Huettel M (2012) The driving forces of porewater and groundwater flow in permeable coastal sediments: A review. Estuar Coast Shelf Sci 98:1–15CrossRefGoogle Scholar
  48. Silbiger N, Nelson C, Remple K, Sevilla J, Quinlan Z, Putnam H, Fox M, Donahue M (2018) Nutrient pollution disrupts key ecosystem functions on coral. Proc R Soc B 285:2–10CrossRefGoogle Scholar
  49. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394CrossRefGoogle Scholar
  50. Schmidt SK, Costello EK, Nemergut DR, Cleveland CC, Reed SC, Weintraub MN, Meyer AF, Martin AM (2007) Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. Ecology 88:1379–1385CrossRefGoogle Scholar
  51. Schoon R, Bissett A, de Beer D (2010) Resilience of pore-water chemistry and calcification in photosynthetic zones of calcifying sediments. Limnol Oceanogr 55:377–385CrossRefGoogle Scholar
  52. Sinutok S, Hill R, Doblin MA, Kühl M, Ralph PJ (2012) Microenvironmental changes support evidence of photosynthesis and calcification inhibition in Halimeda under ocean acidification and warming. Coral Reefs 31:1201–1213CrossRefGoogle Scholar
  53. Sokal, RR, Rohlf FJ (1981) Biometry-the Principles and Practice of Statistics in Biological Research, 4th edition. WH Freeman, New YorkGoogle Scholar
  54. SPSS Inc. (2013) IBM Corp. IBM SPSS Statistics for Windows, Version 22.0. Armonk, NY: IBM CorpGoogle Scholar
  55. Swart PK (1983) Carbon and oxygen isotope fractionation in scleractinian corals: a review. Earth Sci Rev 19:51–80CrossRefGoogle Scholar
  56. Syvitski JPM (1991) Principles, methods, and application of particle size analysis. Cambridge University Press, New YorkCrossRefGoogle Scholar
  57. Tait LW, Schiel DR (2013) Impacts of Temperature on Primary Productivity and Respiration in Naturally Structured Macroalgal Assemblages. PLoS One 8:e74413CrossRefGoogle Scholar
  58. Trnovsky D, Stoltenberg L, Cyronak T, Eyre B (2016) Antagonistic Effects of Ocean Acidification and Rising Sea Surface Temperature on the Dissolution of Coral Reef Carbonate Sediments. Front Mar Sci 3:211CrossRefGoogle Scholar
  59. Warren LA, Maurice PA, Parmar N, Ferris FG (2001) Microbially mediated calcium carbonate precipitation: Implications for Interpreting calcite precipitation and for solid-phase capture of inorganic contaminants. Geomicrobiol J 18:93–115CrossRefGoogle Scholar
  60. Weston NB, Joye SB (2005) Temperature-driven decoupling of key phases of organic matter degradation in marine sediments. Proc Natl Acad Sci U S A 102:17036–17040CrossRefGoogle Scholar
  61. Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYM, Jørgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70CrossRefGoogle Scholar
  62. Wild C, Laforsch C, Huettel M (2006) Detection and enumeration of microbial cells within highly porous calcareous reef sands. Mar Freshw Res 57:415CrossRefGoogle Scholar
  63. Zeebe RE, Westbroek P (2003) A simple model for the CaCO3 saturation state of the ocean: The “Strangelove,” the “Neritan,” and the “Cretan” Ocean. Geochem Geophys Geosyst 4:1–26CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centre for Coastal Biogeochemistry, School of Environment, Science, and EngineeringMilitary Road Southern Cross UniversityLismoreAustralia

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