Coral Reefs

, Volume 34, Issue 1, pp 339–351 | Cite as

Environmental and ecological controls of coral community metabolism on Palmyra Atoll

  • David KoweekEmail author
  • Robert B. Dunbar
  • Justin S. Rogers
  • Gareth J. Williams
  • Nichole Price
  • David Mucciarone
  • Lida Teneva


Accurate predictions of how coral reefs may respond to global climate change hinge on understanding the natural variability to which these ecosystems are exposed and to which they contribute. We present high-resolution estimates of net community calcification (NCC) and net community production (NCP) from Palmyra Atoll, an uninhabited, near-pristine coral reef ecosystem in the central Pacific. In August–October 2012, we employed a combination of Lagrangian and Eulerian frameworks to establish high spatial (~2.5 km2) and temporal (hourly) resolution coral community metabolic estimates. Lagrangian drifts, all conducted during daylight hours, resulted in NCC estimates of −51 to 116 mmol C m−2 h−1, although most NCC estimates were in the range of 0–40 mmol C m−2 h−1. Lagrangian drift NCP estimates ranged from −7 to 67 mmol C m−2 h−1. In the Eulerian setup, we present carbonate system parameters (dissolved inorganic carbon, total alkalinity, pH, and pCO2) at sub-hourly resolution through several day–night cycles and provide hourly NCC and NCP rate estimates. We compared diel cycles of all four carbonate system parameters to the offshore surface water (0–50 m depth) and show large departures from offshore surface water chemistry. Hourly Eulerian estimates of NCC aggregated over the entire study ranged from 14 to 53 mmol C m−2 h−1, showed substantial variability during daylight hours, and exhibited a diel cycle with elevated NCC in the afternoons and depressed, but positive, NCC at night. The Eulerian NCP range was very high (−55 to 177 mmol C m−2 h−1) and exhibited strong variability during daylight hours. Principal components analysis revealed that NCC and NCP were most closely aligned with diel cycle forcing, whereas the NCC/NCP ratio was most closely aligned with reef community composition. Our analysis demonstrates that ecological community composition is the primary determinant of coral reef biogeochemistry on a near-pristine reef and that reef biogeochemistry is likely to be responsive to human behaviors that alter community composition.


Net community calcification Net community production Lagrangian drifts Eulerian measurements Coral reefs Coral ecology 



This manuscript benefitted greatly from the comments of three anonymous reviewers. Helpful conversations with Kevin Arrigo, Andreas Andersson, Stephen Monismith, Hans DeJong, Dan Urban, and Matz Haugen also greatly improved this manuscript. We thank Claire Zabel for her field assistance. We thank The Nature Conservancy for logistical support on Palmyra Atoll as well as the US Fish and Wildlife Service (US FWS) for granting research access. This research was funded by support from the Gordon and Betty Moore Foundation to Robert B. Dunbar. This research was conducted under a permit from the US FWS. This is Palmyra Atoll Research Consortium contribution number 0109. Data from this study have been deposited at the NOAA National Oceanographic Data Center and can be obtained there.

Supplementary material

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  1. Andersson AJ, Mackenzie FT (2004) Shallow-water oceans: a source or sink of atmospheric CO2? Front Ecol Environ 2:348–353Google Scholar
  2. Andersson AJ, Gledhill D (2013) Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Annu Rev Mar Sci 5:321–348CrossRefGoogle Scholar
  3. Anthony KRN, Kleypas JA, Gattuso J-P (2011) Coral reefs modify their seawater carbon chemistry-implications for impacts of ocean acidification. Global Change Biol 17:3655–3666CrossRefGoogle Scholar
  4. Barnes DJ (1983) Profiling coral reef productivity and calcification using pH and oxygen electrodes. J Exp Mar Biol Ecol 66:149–161CrossRefGoogle Scholar
  5. Barnes DJ, Lazar B (1993) Metabolic performance of a shallow reef patch near Eilat on the Red Sea. J Exp Mar Biol Ecol 174:1–13CrossRefGoogle Scholar
  6. Collen JD, Garton DW, Gardner JPA (2009) Shoreline changes and sediment redistribution at Palmyra Atoll (equatorial Pacific Ocean): 1874–Present. J Coast Res 253:711–722CrossRefGoogle Scholar
  7. Collen JD, Baker JA, Dunbar RB, Rieser U, Gardner JPA, Garton DW, Christiansen KJ (2011) The atmospheric lead record preserved in lagoon sediments at a remote equatorial Pacific location: Palmyra Atoll, northern Line Islands. Mar Pollut Bull 62:251–257CrossRefPubMedGoogle Scholar
  8. Dickson AG (1990) Standard potential of the reaction: AgCl(s)+1/2H2(g)=Ag(s)+HCl(aq) and the standard acidity constant of the ion HSO4 - in synthetic sea water from 273.15-K to 318.15-K. J Chem Thermodyn 22:113–127CrossRefGoogle Scholar
  9. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res A 34:1733–1743CrossRefGoogle Scholar
  10. Dickson AG, Afghan JD, Anderson GC (2003) Reference materials for oceanic CO2 analysis: a method for the certification of total alkalinity. Mar Chem 80:185–197CrossRefGoogle Scholar
  11. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. Carbon Dioxide Information Analysis Center, US DOE, Oak Ridge National Laboratory, Oak Ridge, TN, USAGoogle Scholar
  12. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192CrossRefPubMedGoogle Scholar
  13. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan SHC, De’ath G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang 1:165–169CrossRefGoogle Scholar
  14. Falter JL, Lowe RJ, Atkinson MJ, Cuet P (2012) Seasonal coupling and de-coupling of net calcification rates from coral reef metabolism and carbonate chemistry at Ningaloo Reef, Western Australia. J Geophys Res 117:1–14Google Scholar
  15. Falter JL, Lowe RJ, Atkinson MJ, Monismith SG, Schar DW (2008) Continuous measurements of net production over a shallow reef community using a modified Eulerian approach. J Geophys Res 113:1–14Google Scholar
  16. Frankignoulle M, Canon C, Gattuso J-P (1994) Marine calcification as a source of carbon dioxide: positive feedback of increasing atmospheric CO2. Limnol Oceanogr 39:458–462CrossRefGoogle Scholar
  17. Gardner JPA, Garton DW, Collen JD (2010) Near-surface mixing and pronounced deep-water stratification in a compartmentalised, human-disturbed atoll lagoon system. Coral Reefs 30:271–282CrossRefGoogle Scholar
  18. Gattuso J-P, Pichon M, Delesalle B, Frankignoulle M (1993) Community metabolism and air-sea CO2 fluxes in a coral reef ecosystem (Moorea, French Polynesia). Mar Ecol Prog Ser 96:259–267CrossRefGoogle Scholar
  19. Gattuso J-P, 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
  20. Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17CrossRefGoogle Scholar
  21. Ho DT, Law CS, Smith MJ, Schlosser P, Harvey M, Hill P (2006) Measurements of air-sea gas exchange at high wind speeds in the Southern Ocean : Implications for global parameterizations. Geophys Res Lett 33:1–6Google Scholar
  22. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742CrossRefPubMedGoogle Scholar
  23. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas JA, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933CrossRefPubMedGoogle Scholar
  24. Kayanne H, Suzuki A, Saito H (1995) Diurnal changes in the partial pressure of carbon dioxide in coral reef water. Science 269:214–216CrossRefPubMedGoogle Scholar
  25. Kleypas JA, Buddemeier RW, Archer D, Gattuso J-P, Langdon C, Opdyke BN (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120CrossRefPubMedGoogle Scholar
  26. Kline SJ, McClintock FA (1953) Describing uncertainties in single-sample experiments. Mech Eng January:3–8Google Scholar
  27. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434CrossRefPubMedGoogle Scholar
  28. Kroeker KJ, Kordas RL, Crim RN, 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. Global Change Biol 19:1884–1896CrossRefGoogle Scholar
  29. Long MC, Dunbar RB, Tortell PD, Smith WO, Mucciarone DA, Ditullio GR (2011) Vertical structure, seasonal drawdown, and net community production in the Ross Sea, Antarctica. J Geophys Res 116:1–19Google Scholar
  30. McMahon A, Santos IR, Cyronak T, Eyre BD (2013) Hysteresis between coral reef calcification and the seawater aragonite saturation state. Geophys Res Lett 40:4675–4679CrossRefGoogle Scholar
  31. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  32. National Aeronautics and Space Administration, NASA (2007) MERRA 2D IAU Diagnostic, Single Level Meteorology, Time Average 1-hourly. Goddard Space Flight Center, Greenbelt, MD, USAGoogle Scholar
  33. Price NN, Martz TR, Brainard RE, Smith JE (2012) Diel variability in seawater pH relates to calcification and benthic community structure on coral reefs. PLoS One 7:1–9Google Scholar
  34. Reidenbach MA, Monismith SG, Koseff JR, Yahel G (2006) Boundary layer turbulence and flow structure over a fringing coral reef. Limnol Oceanogr 51:1956–1968CrossRefGoogle Scholar
  35. Ricke KL, Orr JC, Schneider K, Caldeira K (2013) Risks to coral reefs from ocean carbonate chemistry changes in recent earth system model projections. Environ Res Lett 8:1–6Google Scholar
  36. Robbins L, Hansen M, Kleypas JA, Meylan S (2010) CO2Calc-a user-friendly seawater carbon calculator for Windows, Mac OS X and iOS (iPhone): U.S. Geological Survey Open-File. Report 2010–1280:17Google Scholar
  37. Rosman JH, Hench JL (2011) A framework for understanding drag parameterizations for coral reefs. J Geophys Res 116:1–15Google Scholar
  38. Sandin SA, Smith JE, Demartini EE, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos JE, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroeder RE, Walsh SM, Jackson JBC, Knowlton N, Sala E (2008) Baselines and degradation of coral reefs in the Northern Line Islands. PLoS One 3:1–11CrossRefGoogle Scholar
  39. Shamberger K, Feely RA, Sabine CL, Atkinson MJ, DeCarlo E, Mackenzie FT, Drupp P, Butterfield D (2011) Calcification and organic production on a Hawaiian coral reef. Mar Chem 127:64–75CrossRefGoogle Scholar
  40. Shaw EC, McNeil BI, Tilbrook B (2012) Impacts of ocean acidification in naturally variable coral reef flat ecosystems. J Geophys Res 117:1–14Google Scholar
  41. Silverman J, Lazar B, Erez J (2007) Effect of aragonite saturation, temperature, and nutrients on the community calcification rate of a coral reef. J Geophys Res 112:1–14Google Scholar
  42. Smith JE, Price NN, Nelson CE, Haas AF (2013) Coupled changes in oxygen concentration and pH caused by metabolism of benthic coral reef organisms. Mar Biol 160:2437–2447CrossRefGoogle Scholar
  43. Smith SV, Key GS (1975) Carbon dioxide and metabolism in marine environments. Limnol Oceanogr 20:493–495CrossRefGoogle Scholar
  44. Stevenson C, Katz LS, Micheli F, Block B, Heiman KW, Perle C, Weng K, Dunbar R, Witting J (2006) High apex predator biomass on remote Pacific islands. Coral Reefs 26:47–51CrossRefGoogle Scholar
  45. Suzuki A, Kawahata H (2003) Carbon budget of coral reef systems: an overview of observations in fringing reefs, barrier reefs and atolls in the Indo-Pacific regions. Tellus B Chem Phys Meterol 55:428–444CrossRefGoogle Scholar
  46. Teneva L, Dunbar RB, Mucciarone DA, Dunckley JF, Koseff JR (2013) High-resolution carbon budgets on a Palau back-reef modulated by interactions between hydrodynamics and reef metabolism. Limnol Oceanogr 58:1851–1870CrossRefGoogle Scholar
  47. van Heuven S, Pierrot D, Rae J, Lewis E, Wallace DWR (2011) MATLAB Program Developed for CO2 System Calculations.
  48. van Hooidonk R, Maynard JA, Planes S (2013) Temporary refugia for coral reefs in a warming world. Nat Clim Chang 3:508–511CrossRefGoogle Scholar
  49. Ware JR, Smith SV, Reaka-Kudla ML (1992) Coral reefs: sources or sinks of atmospheric CO2? Coral Reefs 11:127–130CrossRefGoogle Scholar
  50. Williams GJ, Smith JE, Conklin EJ, Gove JM, Sala E, Sandin SA (2013) Benthic communities at two remote Pacific coral reefs: effects of reef habitat, depth, and wave energy gradients on spatial patterns. PeerJ 1:e81CrossRefPubMedCentralPubMedGoogle Scholar
  51. Zeebe RE, Wolf-Gladrow D (2001) Carbon dioxide in seawater: equilibrium, kinetics, and isotopes. Elsevier Ltd, The NetherlandsGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • David Koweek
    • 1
    Email author
  • Robert B. Dunbar
    • 1
  • Justin S. Rogers
    • 2
  • Gareth J. Williams
    • 3
  • Nichole Price
    • 3
    • 4
  • David Mucciarone
    • 1
  • Lida Teneva
    • 1
    • 5
  1. 1.Department of Environmental Earth System ScienceStanford UniversityStanfordUSA
  2. 2.Department of Civil and Environmental EngineeringStanford UniversityStanfordUSA
  3. 3.Center for Marine Biodiversity and Conservation, Scripps Institution of OceanographyUniversity of California San DiegoLa JollaUSA
  4. 4.Bigelow Laboratory for Ocean SciencesEast BoothbayUSA
  5. 5.Hawai‘i Fish Trust, Betty and Gordon Moore Center for Science and OceansConservation InternationalHonoluluUSA

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