Coral Reefs

pp 1–10 | Cite as

Evaluating measurements of coral reef net ecosystem calcification rates

  • T. A. CourtneyEmail author
  • A. J. Andersson


Monitoring the rates and drivers of coral reef net ecosystem calcification (NEC) under anthropogenic environmental change is critical for predicting associated changes in reef structures and ecosystem services. However, NEC studies to date show weak agreement between studies and notably reveal no relationship between NEC and benthic calcifier cover. In this study, we tested for the sensitivity of calculated NEC to uncertainties in seawater depths and residence times (± 83% relative to 6 m and 6 h, respectively) using a coral reef total alkalinity (AT) simulator (reefCATS) and found that these errors can interact to drive large asymmetric uncertainties ranging from − 91% to + 1000% in NEC. Furthermore, numerical simulations of hypothetical NEC for coral populations occupying reefs with increasing structural complexity (rugosity = 1–4) showed that the effects of reef-scale rugosity on NEC can be as important as benthic community composition. As a result, uncertainties in seawater depth, residence time, and/or reef structural complexity are enough to mask any potential real correlation between NEC and percent calcifier cover in the field. To improve comparability and validity of NEC studies, we recommend that future studies place a high degree of scrutiny on measurements of seawater hydrodynamics, report all NEC equation parameters ± uncertainties, and ideally include benthic community composition and structural complexity data to further explore the relationship between NEC and calcifier cover.


Coral reef Net ecosystem calcification Structural complexity Rugosity Ecosystem services Climate change Biogeochemistry Ecosystem monitoring 



We are grateful to Tyler Cyronak for providing insightful discussions of chemistry-based NEC measurements, Carlos Minces for inspiration of the reefCATS models, and two anonymous reviewers who improved this manuscript with their helpful insights. Funding was provided by NSF DGE-1650112 (TAC) and NSF OCE 12-55042 (AJA). All data from the literature review of previous NEC studies are presented in the supplementary NEC review datasheet.

Author contributions

TAC and AJA conceived the study. TAC constructed the reefCATS model simulations and wrote the first draft of the manuscript with input from AJA.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

338_2019_1828_MOESM1_ESM.xlsx (18 kb)
Supplementary material 1 (XLSX 17 kb)


  1. Albright R, Benthuysen J, Cantin N, Caldeira K, Anthony K (2015) Coral reef metabolism and carbon chemistry dynamics of a coral reef flat. Geophys Res Lett 42:3980–3988CrossRefGoogle Scholar
  2. Andersson AJ, Gledhill D (2013) Ocean Acidification and Coral Reefs: Effects on Breakdown, Dissolution, and Net Ecosystem Calcification. Ann Rev Mar Sci 5:321–348CrossRefGoogle Scholar
  3. Aronson RB, Precht WF (2001) White band diseases and the changing face of Caribbean coral reefs. Hydrobiologia 460:25–38CrossRefGoogle Scholar
  4. Broecker WS, Takahashi T (1966) Calcium carbonate precipitation on the Bahama Banks. J Geophys Res 71:1575CrossRefGoogle Scholar
  5. Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-Pacific: Timing, extent, and subregional comparisons. PLoS One 2:e711CrossRefGoogle Scholar
  6. Chave KE, Smith SV, Roy KJ (1972) Carbonate production by coral reefs. Mar Geol 12:123–140CrossRefGoogle Scholar
  7. Courtney TA, Andersson AJ, Bates NR, Collins A, Cyronak T, de Putron SJ, Eyre BD, Garley R, Hochberg EJ, Johnson R, Musielewicz S, Noyes TJ, Sabine CL, Sutton AJ, Toncin J, Tribollet A (2016) Comparing Chemistry and Census-Based Estimates of Net Ecosystem Calcification on a Rim Reef in Bermuda. Front Mar Sci 3:181CrossRefGoogle Scholar
  8. Courtney TA, De Carlo EH, Page HN, Bahr KD, Barro A, Howins N, Tabata R, Terlouw G, Rodgers KS, Andersson AJ (2018) Recovery of reef-scale calcification following a bleaching event in Kāne’ohe Bay, Hawai’i. Limnol Oceanogr Lett 3:1–9CrossRefGoogle Scholar
  9. Cyronak T, Andersson AJ, Langdon C, Albright R, Bates NR, Caldeira K, Carlton R, Corredor JE, Dunbar RB, Enochs I, Erez J, Eyre BD, Gattuso JP, Gledhill D, Kayanne H, Kline DI, Koweek DA, Lantz C, Lazar B, Manzello D, McMahon A, Meléndez M, Page HN, Santos IR, Schulz KG, Shaw E, Silverman J, Suzuki A, Teneva L, Watanabe A, Yamamoto S (2018) Taking the metabolic pulse of the world’s coral reefs. PLoS One 13:1–17CrossRefGoogle Scholar
  10. DeCarlo TM, Cohen AL, Wong GTF, Shiah F, Lentz SJ, Davis KA, Shamberger KEF, Lohmann P (2017) Community production modulates coral reef pH and the sensitivity of ecosystem calcification to ocean acidification. J Geophys Res Ocean 122:745–761CrossRefGoogle Scholar
  11. Dickson AG, Sabine CL, Christian JR (2007) Guide to Best Practices for Ocean CO2 Measurements. PICES Spec Publ 3(3):191Google Scholar
  12. Edmunds PJ, Comeau S, Lantz C, Andersson A, Briggs C, Cohen A, Gattuso JP, Grady JM, Gross K, Johnson M, Muller EB, Ries JB, Tambutté S, Tambutté E, Venn A, Carpenter RC (2016) Integrating the Effects of Ocean Acidification across Functional Scales on Tropical Coral Reefs. Bioscience 66:350–362CrossRefGoogle Scholar
  13. 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(6378):908–911CrossRefGoogle Scholar
  14. 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 Ocean 113:1–14CrossRefGoogle Scholar
  15. Falter JL, Lowe RJ, Zhang Z, McCulloch M (2013) Physical and Biological Controls on the Carbonate Chemistry of Coral Reef Waters: Effects of Metabolism, Wave Forcing, Sea Level, and Geomorphology. PLoS One 8(1):e53303CrossRefGoogle Scholar
  16. Gardner TA, Côté IM, Gill JA, Grant A, Watkinson AR (2003) Long-Term Region-Wide Declines in Caribbean Corals. Science 301(5635):958–960CrossRefGoogle Scholar
  17. 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
  18. Goatley CHR, Bellwood DR (2011) The roles of dimensionality, canopies and complexity in ecosystem monitoring. PLoS One 6:e27307CrossRefGoogle Scholar
  19. Graham NAJ, Nash KL (2013) The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315–326CrossRefGoogle Scholar
  20. Harris DL, Rovere A, Casella E, Power H, Canavesio R, Collin A, Pomeroy A, Webster JM, Parravicini V (2018) Coral reef structural complexity provides important coastal protection from waves under rising sea levels. Sci Adv 4(2):eaao4350Google Scholar
  21. Hubbard DK, Miller AI, Scaturo D (1990) Production and cycling of calcium carbonate in a shelf-edge reef system (St. Croix, U.S. Virgin Islands): Applications to the nature of reef systems in the fossil record. J Sediment Petrol 60:335–360Google Scholar
  22. Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G, McWilliam MJ, Pears RJ, Pratchett MS, Skirving WJ, Stella JS, Torda G (2018) Global warming transforms coral reef assemblages. Nature 556(7702):492CrossRefGoogle Scholar
  23. Jackson JBC, Donovan MK, Cramer KL, Lam V (2014) Status and Trends of Caribbean Coral Reefs : 1970–2012. IUCN, Glob Coral Reef Monit NetwGoogle Scholar
  24. Kinsey DW (1979) Carbon turnover and accumulation by coral reefs. Doctoral dissertation, University of Hawai'iGoogle Scholar
  25. Kinsey DW (1981) The Pacific/Atlantic reef growth controversy. Proc Fourth Int Coral Reef Symp Manila 1:493–498Google Scholar
  26. Kinsey DW (1985) Metabolism, calcification and carbon production: 1 systems level studies. Fifth Int Coral Reef Congr 4:505–526Google Scholar
  27. Kleypas JA, Buddemeier RW, Gattuso JP (2001) The future of coral reefs in an age of global change. Int J Earth Sci 90:426–437CrossRefGoogle Scholar
  28. Langdon C, Gattuso J-P, Andersson A (2010) Measurements of calcification and dissolution of benthic organisms and communities. Guide to Best Pract Ocean Acidif Res Data Report 213–232Google Scholar
  29. Long MH, Charette MA, Martin WR, Mccorkle DC (2015) Oxygen metabolism and pH in coastal ecosystems: Eddy Covariance Hydrogen ion and Oxygen Exchange System (ECHOES). Limnol Oceanography Methods 13:438–450CrossRefGoogle Scholar
  30. Lowe RJ, Falter JL (2015) Oceanic Forcing of Coral Reefs. Ann Rev Mar Sci 7:43–66CrossRefGoogle Scholar
  31. Lowe RJ, Falter JL, Monismith SG, Atkinson MJ (2009) A numerical study of circulation in a coastal reef-lagoon system. J Geophys Res Ocean 114:1–18CrossRefGoogle Scholar
  32. McDougall TJ, Barker PM (2011) Getting started with TEOS-10 and the Gibbs Seawater (GSW) Oceanographic Toolbox. SCOR/IAPSO WG127Google Scholar
  33. McWilliam M, Hoogenboom MO, Baird AH, Kuo C, Madin JS, Hughes TP (2018) Biogeographical disparity in the functional diversity and redundancy of corals. Proc Natl Acad Sci 115(12):3084–3089CrossRefGoogle Scholar
  34. Montaggioni LFF (2005) History of Indo-Pacific coral reef systems since the last glaciation: Development patterns and controlling factors. Earth-Science Rev 71:1–75CrossRefGoogle Scholar
  35. Montaggioni LF, Braithwaite CJR (2009) Quaternary coral reef systems: history, development processes and controlling factors. Elsevier 5Google Scholar
  36. Morgan KM, Kench PS (2012) Skeletal extension and calcification of reef-building corals in the central Indian Ocean. Mar Environ Res 81:78–82CrossRefGoogle Scholar
  37. Muehllehner N, Langdon C, Venti A, Kadko D (2016) Dynamics of carbonate chemistry, production, and calcification of the Florida Reef Tract (2009–2010): Evidence for seasonal dissolution. Global Biogeochem Cycles 30:661–688CrossRefGoogle Scholar
  38. Page HN, Courtney TA, Collins A, De Carlo EH, Andersson AJ (2017) Net Community Metabolism and Seawater Carbonate Chemistry Scale Non-Intuitively with Coral Cover. Front Mar Sci 4:1–17CrossRefGoogle Scholar
  39. Perry CT, Edinger EN, Kench PS, Murphy GN, Smithers SG, Steneck RS, Mumby PJ (2012) Estimating rates of biologically driven coral reef framework production and erosion: A new census-based carbonate budget methodology and applications to the reefs of Bonaire. Coral Reefs 31:853–868CrossRefGoogle Scholar
  40. Perry CT, Steneck RS, Murphy GN, Kench PS, Edinger EN, Smithers SG, Mumby PJ (2015) Regional-scale dominance of non-framework building corals on Caribbean reefs affects carbonate production and future reef growth. Glob Chang Biol 21:1153–1164CrossRefGoogle Scholar
  41. Perry CT, Alvarez-Filip L, Graham NA, Mumby PJ, Wilson SK, Kench PS, Manzello DP, Morgan KM, Slangen AB, Thomson DP, Januchowski-Hartley F (2018) Loss of coral reef growth capacity to track future increases in sea-level. Nature 558(7710):396CrossRefGoogle Scholar
  42. Pichon M (1997) Coral reef metabolism in the Indo-Pacific: the broader picture. 8th Int Coral Reef Symp 1:977–980Google Scholar
  43. Pratchett MS, Anderson KD, Hoogenboom MO, Widman E, Baird AH, Pandolfi JM, Edmunds PJ, Lough JM (2015) Spatial, temporal and taxonomic variation in coral growth - implications for the structure and function of coral reef ecosystems. Oceanogr Mar Biol An Annu Rev 53:215–296Google Scholar
  44. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria URL: http// Scholar
  45. Richardson LE, Graham NAJ, Hoey AS (2017) Cross-scale habitat structure driven by coral species composition on tropical reefs. Sci Rep 7:7557CrossRefGoogle Scholar
  46. Roquet F, Madec G, Mcdougall TJ, Barker PM (2015) Accurate polynomial expressions for the density and specific volume of seawater using the TEOS-10 standard. Ocean Model 90:29–43CrossRefGoogle Scholar
  47. Shamberger KEF, Feely RA, Sabine CL, Atkinson MJ, DeCarlo EH, Mackenzie FT, Drupp PS, Butterfield DA (2011) Calcification and organic production on a Hawaiian coral reef. Mar Chem 127:64–75CrossRefGoogle Scholar
  48. 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 Ocean. Google Scholar
  49. Silverman J, Lazar B, Cao L, Caldeira K, Erez J (2009) Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys Res Lett 36:1–5CrossRefGoogle Scholar
  50. Smith SV, Key GS (1975) Carbon Dioxide and Metabolism in Marine Environments. Limnol Oceanogr 20:493–495CrossRefGoogle Scholar
  51. Soetaert K, Petzoldt T, Setzer RW (2010) Package deSolve: Solving Initial Value Differential Equations in R. J Stat SoftwGoogle Scholar
  52. Stearn W, Scoffin TP, Martindale W (1977) Calcium carbonate budget of a fringing reef on the west coast of Barbados. Bull Mar Sci 27:479–510Google Scholar
  53. Storlazzi CD, Gingerich SB, Van Dongeren A, Cheriton OM, Swarzenski PW, Quataert E, Voss CI, Field DW, Annamalai H, Piniak GA, McCall R (2018) Most atolls will be uninhabitable by the mid-21st century because of sea-level rise exacerbating wave-driven flooding. Sci Adv 4: eaap9741Google Scholar
  54. Szmant AM (1997) Nutrient effects on coral reefs: a hypothesis on the importance of topographic and trophic complexity to reef nutrient dynamics. Proc 8th Int Coral Reef Symp, Panama 1527–1532Google Scholar
  55. Szmant AM (2002) Nutrient Enrichment on Coral Reefs: Is It a Major Cause of Coral Reef Decline? Estuaries 25:743–766CrossRefGoogle Scholar
  56. Takeshita Y, Mcgillis W, Briggs EM, Carter AL, Donham EM, Martz TR, Price NN, Smith JE (2016) Assessment of net community production and calcification of a coral reef using a boundary layer approach. J Geophys Res Ocean 121:5655–5671CrossRefGoogle Scholar
  57. Tanner E (1995) Competition between scleractinian corals and macroalgae: An experimental investigation of coral growth, survival and reproduction. Journal of Experimental Marine Biology and Ecology 190:151–168CrossRefGoogle Scholar
  58. Tanner JE (1997) Interspecific competition reduces fitness in scleractinian corals. Journal of Experimental Marine Biology and Ecology 214:19–34CrossRefGoogle Scholar
  59. Venti A, Kadko D, Andersson AJ, Langdon C, Bates NR (2012) A multi-tracer model approach to estimate reef water residence times. Limnol Oceanogr Methods 10:1078–1095CrossRefGoogle Scholar
  60. Yates KK, Zawada DG, Smiley NA, Tiling-Range G (2017) Divergence of seafloor elevation and sea level rise in coral reef ecosystems. Biogeosciences 14:1739–1772CrossRefGoogle Scholar
  61. Zhang Z, Falter J, Lowe R, Ivey G (2012) The combined influence of hydrodynamic forcing and calcification on the spatial distribution of alkalinity in a coral reef system. J Geophys Res Ocean 117:1–18Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Scripps Institution of OceanographyUniversity of California, San DiegoLa JollaUSA

Personalised recommendations