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Coral calcification under environmental change: a direct comparison of the alkalinity anomaly and buoyant weight techniques

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Abstract

Two primary methods—the buoyant weight (BW) and alkalinity anomaly (AA) techniques—are currently used to quantify net calcification rates (G) in scleractinian corals. However, it remains unclear whether they are directly comparable since the few method comparisons conducted to date have produced inconsistent results. Further, such a comparison has not been made for tropical corals. We directly compared G BW and G AA in four tropical and one temperate coral species cultured under various pCO2, temperature, and nutrient conditions. A range of protocols for conducting alkalinity depletion incubations was assessed. For the tropical corals, open-top incubations with manual stirring produced G AA that were highly correlated with and not significantly different from G BW. Similarly, G AA of the temperate coral was not significantly different from G BW when incubations provided water motion using a pump, but were significantly lower than G BW by 16% when water motion was primarily created by aeration. This shows that the two techniques can produce comparable calcification rates in corals but only when alkalinity depletion incubations are conducted under specific conditions. General recommendations for incubation protocols are made, especially regarding adequate water motion and incubation times. Further, the re-analysis of published data highlights the importance of using appropriate regression statistics when both variables are random and measured with error. Overall, we recommend the AA technique for investigations of community and short-term day versus night calcification, and the BW technique to measure organism calcification rates integrated over longer timescales due to practical limitations of both methods. Our findings will facilitate the direct comparison of studies measuring coral calcification using either method and thus have important implications for the fields of ocean acidification research and coral biology in general.

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References

  • Anthony KRN, Kleypas JA, Gattuso J-P (2011) Coral reefs modify their seawater carbon chemistry — implications for impacts of ocean acidification. Glob Chang Biol 17:3655–3666

    Article  Google Scholar 

  • Bak RPM (1973) Coral weight increment in situ. A new method to determine coral growth. Mar Biol 20:45–49

    Article  Google Scholar 

  • Broecker WS, Takahashi T (1966) Calcium carbonate precipitation on the Bahama Banks. J Geophys Res 71:1575–1602

    Article  CAS  Google Scholar 

  • Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365

    Article  CAS  PubMed  Google Scholar 

  • Cantin NE, Cohen AL, Karnauskas KB, Tarrant AM, McCorkle DC (2010) Ocean warming slows coral growth in the central Red Sea. Science 329:322–325

    Article  CAS  PubMed  Google Scholar 

  • Chan NCS, Connolly SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob Chang Biol 19:282–290

    Article  PubMed  Google Scholar 

  • Chisholm JRM, Gattuso J-P (1991) Validation of the alkalinity anomaly technique for investigating calcification of photosynthesis in coral reef communities. Limnol Oceanogr 36:1232–1239

    Article  CAS  Google Scholar 

  • Comeau S, Carpenter RC, Edmunds PJ (2013) Coral reef calcifiers buffer their response to ocean acidification using both bicarbonate and carbonate. Proc R Soc Lond B Biol Sci 280:20122374

    Article  CAS  Google Scholar 

  • Comeau S, Edmunds PJ, Lantz CA, Carpenter RC (2014a) Water flow modulates the response of coral reef communities to ocean acidification. Sci Rep 4:06681

    Article  CAS  Google Scholar 

  • Comeau S, Carpenter RC, Nojiri Y, Putnam HM, Sakai K, Edmunds PJ (2014b) Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification. Proc R Soc Lond B Biol Sci 281:20141339

    Article  Google Scholar 

  • Dennison WC, Barnes DJ (1988) Effect of water motion on coral photosynthesis and calcification. J Exp Mar Bio Ecol 115:67–77

    Article  Google Scholar 

  • Gazeau F, Urbini L, Cox TE, Alliouane S, Gattuso JP (2015) Comparison of the alkalinity and calcium anomaly techniques to estimate rates of net calcification. Mar Ecol Prog Ser 527:1–12

    Article  Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck R, 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 318:1737–1742

    Article  CAS  PubMed  Google Scholar 

  • Holcomb M, McCorkle DC, Cohen AL (2010) Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander, 1786). J Exp Mar Bio Ecol 386:27–33

    Article  Google Scholar 

  • Holcomb M, Cohen AL, McCorkle DC (2012) An investigation of the calcification response of the sceractinian coral Astrangia poculata to elevated pCO2 and the effects of nutrients, zooxanthellae and gender. Biogeosciences 9:29–39

    Article  CAS  Google Scholar 

  • Holcomb M, Tambutté E, Allemand D, Tambutté S (2014) Light enhanced calcification in Stylophora pistillata: effects of glucose, glycerol and oxygen. PeerJ 2:e375

    Article  PubMed  PubMed Central  Google Scholar 

  • Jacques TG, Pilson MEQ (1980) Experimental ecology of the temperate scleractinian coral Astrangia danae I. Partition of respiration, photosynthesis and calcification between host and symbionts. Mar Biol 60:167–178

    Article  CAS  Google Scholar 

  • Jokiel PL (1978) Effect of water motion on reef corals. J Exp Mar Bio Ecol 35:87–97

    Article  Google Scholar 

  • Jokiel PL, Maragos JE, Franzisket L (1978) Coral growth: buoyant weight technique. In: Stoddart DR, Johannes RE (eds) Coral reefs: resesarch methods. UNESCO, Paris, pp 529–541

    Google Scholar 

  • Kleypas J, Buddemeier RW, Archer D, Gattuso J-P, Langdon C, Opdyke BN (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120

    Article  CAS  PubMed  Google Scholar 

  • Langdon C, Takahashi T, Sweeney C, Chipman D, Goddard J, Marubini F, Aceves H, Barnett H (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochem Cycles 14:639–654

    Article  CAS  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical Ecology. Elsevier, Amsterdam

    Google Scholar 

  • Maier C, Schubert A, Berzunza Sànchez MM, Weinbauer MG, Watremez P, Gattuso J-P (2013) End of the century pCO2 levels do not impact calcification in Mediterranean cold-water corals. PLoS One 8:e62655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marubini F, Ferrier-Pages C, Cuif J-P (2003) Suppression of skeletal growth in scleractinian corals by decreasing ambient carbonate-ion concentration: a cross-family comparison. Proc R Soc Lond B Biol Sci 270:179–184

    Article  Google Scholar 

  • Marubini F, Barnett H, Langdon C, Atkinson MJ (2001) Dependence of calcification on light and carbonate ion concentration for the hermatypic coral Porites compressa. Mar Ecol Prog Ser 220:153–162

    Article  CAS  Google Scholar 

  • Murillo LJA, Jokiel PL, Atkinson MJ (2014) Alkalinity to calcium flux ratios for corals and coral reef communities: variances between isolated and community conditions. PeerJ 2:e249

    Article  PubMed  PubMed Central  Google Scholar 

  • Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422

    Article  CAS  PubMed  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, New York

    Book  Google Scholar 

  • Riebesell U, Fabry VJ, Hansson L, Gattuso JP (2010) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourg

    Google Scholar 

  • Rodolfo-Metalpa R, Martin S, Ferrier-Pages C, Gattuso J-P (2010) Response of the temperate coral Cladocora caespistosa to mid- and long-term exposure to pCO2 and temperature levels projected for the year 2100 AD. Biogeosciences 7:289–300

    Article  CAS  Google Scholar 

  • Sabine CL, Feely RF, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng T-H, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371

    Article  CAS  PubMed  Google Scholar 

  • Schoepf V, Grottoli AG, Warner M, Cai W-J, Melman TF, Hoadley KD, Pettay DT, Hu X, Li Q, Xu H, Wang Y, Matsui Y, Baumann J (2013) Coral energy reserves and calcification in a high-CO2 world at two temperatures. PLoS One 8:e75049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sebens KP, Helmuth B, Carrington E, Agius B (2003) Effects of water flow on growth and energetics of the scleractinian coral Agaricia tenuifolia in Belize. Coral Reefs 22:35–47

    Google Scholar 

  • Smith SV, Pesret F (1974) Processes of carbon dioxide flux in the Fanning Atoll lagoon. Pac Sci 48:225–245

    Google Scholar 

  • Smith SV, Key GS (1975) Carbon dioxide and metabolism in marine environments. Limnol Oceanogr 20:493–495

    Article  CAS  Google Scholar 

  • Smith SV, Kinsey DW (1978) Calcification and organic carbon metabolism as indicated by carbon dioxide. In: Stoddart DR, Johannes RE (eds) Coral reefs: research methods. United Nations, Paris, pp 469–485

    Google Scholar 

  • Spencer Davies P (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395

    Article  Google Scholar 

  • Steller DL, Hernández-Ayón JM, Cabello-Pasini A (2007) Effect of temperature on photosynthesis, growth and calcification rates of the free-living coralline alga Lithophyllum margaritae. Ciencias Marinas 33:441–456

    CAS  Google Scholar 

  • Tambutté E, Allemand D, Bourge I, Gattuso JP, Jaubert J (1995) An improved 45Ca protocol for investigating physiological mechanisms in coral calcification. Mar Biol 122:453–459

    Article  Google Scholar 

Download references

Acknowledgments

We thank all staff at Reef Systems Coral Farm for logistical support. We thank E. Zebrowski, M. Berzelis, M. Ringwald, S. Levas, and S. Blackhurst at The Ohio State University for their assistance in the field and in the laboratory. We thank Jimmie (Luke) Snaric for carrying out the CO2 degassing experiment at Texas A&M University Corpus Christi. This work was supported by funding from the US National Science Foundation (NSF-EF-1041124, 1040940, 1041070 to AGG, MEW, and WJC, respectively). QL and HX acknowledge the partial support of their respective home institutions for their visit of the Cai laboratory at the University of Georgia when part of this work was accomplished. XH was a postdoctoral researcher in WJC’s laboratory at the University of Georgia during the experimental portion of this work, and also acknowledges the startup support provided by the College of Science and Engineering, Texas A&M University—Corpus Christi during the preparation of this manuscript. At WHOI, this work benefited from the assistance of B. Belastock, M. Brosnahan, N. Cantin, A. Cohen, G. Gaetani, S. Gallager, P. Henderson, K. Hoering, F. Keller, D. McCorkle, C. McGraw, J. Ries, T. Rioux, N. Shimizu, R. Schenk, J. Smith, A. Tarrant, K. Thompson, N. Trowbridge, A. Wang, D. Wellwood, M. White, and A. York. This material is based upon work supported under a US National Science Foundation Graduate Research Fellowship and International Society for Reef Studies/Ocean Conservancy Fellowship awarded to MH, and an NSF Grant (Oce-1041106) awarded to Anne Cohen.

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Author notes

  1. Justin H. Baumann

    Present address: Department of Marine Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

Authors and Affiliations

  1. School of Earth Sciences, The Ohio State University, Columbus, OH, USA

    Verena Schoepf, Yohei Matsui, Justin H. Baumann & Andréa G. Grottoli

  2. ARC Centre of Excellence for Coral Reef Studies, UWA Oceans Institute and School of Earth and Environment, University of Western Australia, Crawley, WA, Australia

    Verena Schoepf & Michael Holcomb

  3. Department of Physical and Environmental Sciences, Texas A&M University – Corpus Christi, Corpus Christi, TX, USA

    Xinping Hu

  4. Department of Marine Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, MA, USA

    Michael Holcomb

  5. School of Marine Science and Policy, University of Delaware, Newark, DE, USA

    Wei-Jun Cai

  6. Department of Marine Sciences, The University of Georgia, Athens, GA, USA

    Wei-Jun Cai, Qian Li, Yongchen Wang & Hui Xu

  7. State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, China

    Qian Li

  8. Department of Marine Science, Zhejiang University, Hangzhou, Zhejiang, China

    Hui Xu

  9. School of Marine Science and Policy, University of Delaware, Lewes, DE, USA

    Mark E. Warner, Kenneth D. Hoadley & D. Tye Pettay

  10. Reef Systems Coral Farm, New Albany, OH, USA

    Todd F. Melman

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  1. Verena Schoepf
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  8. Mark E. Warner
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  9. Todd F. Melman
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Corresponding authors

Correspondence to Verena Schoepf or Xinping Hu.

Additional information

Communicated by Biology Editor Prof. Mark R. Patterson

Verena Schoepf and Xinping Hu have contributed equally to this manuscript.

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Schoepf, V., Hu, X., Holcomb, M. et al. Coral calcification under environmental change: a direct comparison of the alkalinity anomaly and buoyant weight techniques. Coral Reefs 36, 13–25 (2017). https://doi.org/10.1007/s00338-016-1507-z

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  • DOI: https://doi.org/10.1007/s00338-016-1507-z

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