Coral Reefs

, Volume 34, Issue 2, pp 451–460 | Cite as

Responses of the tropical gorgonian coral Eunicea fusca to ocean acidification conditions

  • C. E. Gómez
  • V. J. Paul
  • R. Ritson-Williams
  • N. Muehllehner
  • C. Langdon
  • J. A. SánchezEmail author


Ocean acidification can have negative repercussions from the organism to ecosystem levels. Octocorals deposit high-magnesium calcite in their skeletons, and according to different models, they could be more susceptible to the depletion of carbonate ions than either calcite or aragonite-depositing organisms. This study investigated the response of the gorgonian coral Eunicea fusca to a range of CO2 concentrations from 285 to 4,568 ppm (pH range 8.1–7.1) over a 4-week period. Gorgonian growth and calcification were measured at each level of CO2 as linear extension rate and percent change in buoyant weight and calcein incorporation in individual sclerites, respectively. There was a significant negative relationship for calcification and CO2 concentration that was well explained by a linear model regression analysis for both buoyant weight and calcein staining. In general, growth and calcification did not stop in any of the concentrations of pCO2; however, some of the octocoral fragments experienced negative calcification at undersaturated levels of calcium carbonate (>4,500 ppm) suggesting possible dissolution effects. These results highlight the susceptibility of the gorgonian coral E. fusca to elevated levels of carbon dioxide but suggest that E. fusca could still survive well in mid-term ocean acidification conditions expected by the end of this century, which provides important information on the effects of ocean acidification on the dynamics of coral reef communities. Gorgonian corals can be expected to diversify and thrive in the Atlantic–Eastern Pacific; as scleractinian corals decline, it is likely to expect a shift in these reef communities from scleractinian coral dominated to octocoral/soft coral dominated under a “business as usual” scenario of CO2 emissions.


Ocean acidification Carbonate saturation state Tropical gorgonian Caribbean Calcein 



The Smithsonian Institution Scholarly Studies Program and the Smithsonian Marine Station at Fort Pierce (SMSFP) through the Hunterdon Oceanographic Endowment funded this study. Additional support was received from the Coral and Climate Change Laboratory (RSMAS-University of Miami) for use of the CO2 system as well as Facultad de Ciencias, Universidad de los Andes and COLCIENCIAS (1204-521-28867). We greatly appreciate the collaboration of SMSFP staff, H. Reichardt, J. Piraino, S. Reed. Special thanks to S. Gunasekera, M. Boyle, J. Craft and W. Hoffman (SMSFP) and C. Mor and R. Okasaki (University of Miami). We thank Simon Davy and two anonymous reviewers for their constructive comments that greatly improved this manuscript. This is contribution #968 of the SMSFP.


  1. Agegian C (1985) The biogeochemical ecology of Porolithon gardineri (Foslie). Ph.D thesis, University of Hawaii, p 178Google Scholar
  2. Allemand D, Bénazet-Tambutté S (1996) Dynamics of calcification in the Mediterranean red coral Corallium rubrum (Linnaeus) (Cnidaria, Octocorallia). J Exp Zool 276:270–278CrossRefGoogle Scholar
  3. Andersson A, Bates N, Mackenzie F (2007) Dissolution of carbonate sediments under rising pCO2 and ocean acidification: observations from Devil’s Hole, Bermuda. Aquat Geochem 13:237–264CrossRefGoogle Scholar
  4. Bayer F (1961) The shallow water octocorallia of the West Indian region: a manual for marine biologist. Martinus Nijhoff, The Hague, p 373Google Scholar
  5. Bramanti L, Movilla J, Guron M, Calvo E, Gori A, Dominguez-Carrió C, Grinyó J, Lopez-Sanz A, Martinez-Quintana A, Pelejero C, Ziveri P, Rossi S (2013) Detrimental effects of ocean acidification on the economically important Mediterranean red coral (Corallium rubrum). Global Change Biol 19:1897–1908CrossRefGoogle Scholar
  6. Caldeira K, Wickett M (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefPubMedGoogle Scholar
  7. Cary LR (1918) The gorgonacea as a factor in the formation of coral reefs. Carnegie Inst Wash Publications 213:341–362Google Scholar
  8. Chan NCS, Connolly SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Global Change Biol 19:282–290CrossRefGoogle Scholar
  9. Chave K, Deffeyes K, Weyl P, Garrels R, Thompson M (1962) Observations on the solubility of skeletal carbonates in aqueous solutions. Science 137:33–34CrossRefPubMedGoogle Scholar
  10. Cohen A, McConnaughey T (2003) Geochemical perspectives on coral mineralization. In: Dove P, Weiner S, De Yoreo J (eds) Biomineralization: Reviews in mineralogy and Geochemistry. Mineralogical Society of America, Chantilly, VA, pp 151–187Google Scholar
  11. Comeau S, Carpenter RC, Edmunds PJ (2013) Coral reef calcifiers buffer their response to ocean acidification using both bicarbonate and carbonate. Proc R Soc B: Biol Sci 280:20122374CrossRefGoogle Scholar
  12. Crook ED, Cohen AL, Rebolledo-Vieyra M, Hernandez L, Paytan A (2013) Reduced calcification and lack of acclimatization by coral colonies growing in areas of persistent natural acidification. Proc Natl Acad Sci USA 110:11044–11049CrossRefPubMedCentralPubMedGoogle Scholar
  13. Davies SP (1989) Short-term growth measurement of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395CrossRefGoogle Scholar
  14. Dickson AG (1990) Standard potential of the reaction: AgCl(s) + 1/2 H2(g) = Ag(s) + HCl(aq), and the standard acidity constant of the ion HSO4- in synthetic seawater from 273.15 to 318.15 K. J Chem Thermodynamics 22:113–127CrossRefGoogle Scholar
  15. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res 34:1733–1743CrossRefGoogle Scholar
  16. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication 3:191Google Scholar
  17. Doney SC (2010) The growing human footprint on coastal and open-ocean biogeochemistry. Science 328:1512–1516CrossRefPubMedGoogle Scholar
  18. Dupont S, Havenhand J, Thorndyke W, Peck L, Thorndyke M (2008) Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Mar Ecol Prog Ser 373:285–294CrossRefGoogle Scholar
  19. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, 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 Climate Change 1:165–169CrossRefGoogle Scholar
  20. Gabay Y, Benayahu Y, Fine M (2013) Does elevated pCO2 affect reef octocorals? Ecol Evol 3:465–473CrossRefPubMedCentralPubMedGoogle Scholar
  21. Gabay Y, Fine M, Barkay Z, Benayahu Y (2014) Octocoral tissue provides protection from declining oceanic pH. PLoS One 9(4):e91553CrossRefPubMedCentralPubMedGoogle Scholar
  22. Gao K, Zheng Y (2010) Combined effects of ocean acidification and solar UV radiation on photosynthesis, growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta). Global Change Biol 16:2388–2398CrossRefGoogle Scholar
  23. Gao K, Aruga Y, Asada K, Ishihara T, Akano T, Kiyohara M (1993) Calcification in the articulated coralline alga Corallina pilulifera, with special reference to the effect of elevated CO2 concentration. Mar Biol 117:129–132CrossRefGoogle Scholar
  24. Gattuso J-P, Frankignoulle M, Bourge I, Romaine S, Buddemeier R (1998) Effect of calcium carbonate saturation of seawater on coral calcification. Global Planet Change 18:37–46CrossRefGoogle Scholar
  25. Goh NK, Peter KL, Chou L (1999) Notes on the shallow water gorgonian-associated fauna on coral reefs in Singapore. Bull Mar Sci 655:259–282Google Scholar
  26. Goldberg W, Benayahu Y (1987) Spicule formation in the gorgonian coral Pseudoplexaura flagellosa 1: Demonstration of intracellular and extracellular growth and the effect of ruthenium red during decalcification. Bull Mar Sci 40:287–303Google Scholar
  27. Harvell CD, Fenical W, Greene CH (1988) Chemical and structural defenses of Caribbean gorgonians (Pseudopterogorgia spp.). I. Development and in situ feeding assay. Mar Ecol Prog Ser 49:287–294CrossRefGoogle Scholar
  28. Hoegh-Guldberg O, Mumby P, Hooten A, Steneck R, Greenfield P, Gomez E, Harvell C, Sale P, Edwards A, Caldeira K, Knowlton N, Eakin C, Iglesias-Prieto R, Muthiga M, Bradbury R, Dubi A, Hatziolos M (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742CrossRefPubMedGoogle Scholar
  29. Inoue S, Kayanne H, Yamamoto S, Kurihara H (2013) Spatial community shift from hard to soft corals in acidified water. Nat Climate Change 3:683–687CrossRefGoogle Scholar
  30. IPCC (2013) Climate change 2013: the physical science basis. Working group I contribution to the fifth assessment report on the intergovernmental panel on climate change. Stockholm, Sweden, p 1552Google Scholar
  31. Jeng MS, Huang HD, Dai CF, Hsiao YC, Benayahu Y (2011) Sclerite calcification and reef-building in the fleshy octocoral genus Sinularia (Octocorallia: Alcyonacea). Coral Reefs 30:925–933CrossRefGoogle Scholar
  32. Jokiel P, Rodgers K, Kuffner I, Andersson A, Cox E, Mackenzie F (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27:473–483CrossRefGoogle Scholar
  33. Kingsley R, Watabe N (1989) The dynamics of spicule calcification in whole colonies of the gorgonian Leptogorgia virgulata. J Exp Mar Biol Ecol 133:57–65CrossRefGoogle Scholar
  34. Kleypas J, Buddemeier R, Archer D, Gattuso J-P, Langdon C, Opdyke B (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120CrossRefPubMedGoogle Scholar
  35. Krief S, Hendy EJ, Fine M, Yam R, Meibom A, Foster GL, Shemesh A (2010) Physiological and isotopic responses of scleractinian corals to ocean acidification. Geochim Cosmochim Acta 74:4988–5001CrossRefGoogle Scholar
  36. 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
  37. Kuffner I, Andersson A, Jokiel P, Rodgers K, Mackenzie F (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117CrossRefGoogle Scholar
  38. Kuffner IB, Grober-Dunsmore R, Brock JC, Hickey TD (2010) Biological community structure on patch reefs in Biscayne National Park, FL, USA. Environ Monit Assess 164:513–531CrossRefPubMedGoogle Scholar
  39. Langdon C, Atkinson M (2005) Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res 110:C09S07Google Scholar
  40. Lepore M, Penchaszadeh P, Alfaya J, Herrmann M (2009) Aplicación de calceina para la estimación del crecimiento de la almeja amarilla Mesodesma mactroides Reeve, 1854. Rev Biol Mar Oceanogr 44:767–774CrossRefGoogle Scholar
  41. Lewis JC, Von Wallis E (1991) The function of surface sclerites in gorgonians (Coelenterata, Octocorallia). Biol Bull 181:275–288CrossRefGoogle Scholar
  42. Lucas J, Knapp L (1997) A physiological evaluation of carbon sources for calcification in the octocoral Leptogorgia virgulata (Lamarck). J Exp Biol 200:2653–2662PubMedGoogle Scholar
  43. Manzello DP (2010) Coral growth with thermal stress and ocean acidification: lessons from the eastern tropical Pacific. Coral Reefs 29:749–758CrossRefGoogle Scholar
  44. Marschal C, Garrabou J, Harmelin J, Pichon M (2004) A new method for measuring growth and age in the precious red coral Corallium rubrum (L.). Coral Reefs 23:423–432CrossRefGoogle Scholar
  45. Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Global Change Biol 15:2089–2100CrossRefGoogle Scholar
  46. Mehrbach C, Culberson H, 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
  47. Morales-Pinzón A, Orkisz M, Rodríguez-Useche CM, Torres-Gonzáles JS, Teillaud S, Sánchez JA, Hernández-Hoyos M (2014) A semi-automatic method to extract canal pathways in 3D micro-CT images of octocorals. PLoS One 9(1):e85557CrossRefPubMedCentralPubMedGoogle Scholar
  48. Morse J, Andersson A, Mackenzie F (2006) Initial responses of carbonate-rich shelf sediments to rising atmospheric pCO2 and “ocean acidification”: Role of high Mg-calcites. Geochim Cosmochim Acta 70:5814–5830CrossRefGoogle Scholar
  49. Nagelkerken I, Dorenbosch M, Verberk WCEP, Morinière ECDL, Velde GVD (2000) Importance of shallow-water biotopes of a Caribbean bay for juvenile coral reef fishes: patterns in biotope association, community structure and spatial distribution. Mar Ecol Prog Ser 202:175–192CrossRefGoogle Scholar
  50. Pierrot D, Lewis E, Wallace DWR (2006) MS Excel Program Developed for CO2 System Calculations ORNL/CDIAC‐105, Carbon Dioxide Inf. Anal. Cent., Oak Ridge Natl. Lab., U. S. Dept. of Energy, Oak Ridge, TNGoogle Scholar
  51. Purcell S, Blockmans B (2009) Effective fluorochrome marking of juvenile sea cucumbers for sea ranching and restocking. Aquaculture 296:263–270CrossRefGoogle Scholar
  52. Ries J, Cohen A, McCorkle D (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134CrossRefGoogle Scholar
  53. Ries J, Cohen A, McCorkle D (2010) A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. Coral Reefs 29:661–674CrossRefGoogle Scholar
  54. Rodolfo-Metalpa R, Houlbrèque F, Tambutté É, Boisson F, Baggini C, Patti FP, Jeffree R, Fine M, Foggo A, Gattuso J-P, Hall-Spencer JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Climate Change 1:308–312CrossRefGoogle Scholar
  55. Ruzicka RR, Colella MA, Porter JW, Morrison JM, Kidney JA, Brinkhuis V, Lunz KS, Macaulay KA, Bartlett LA, Meyers MK, Colee J (2013) Temporal changes in benthic assemblages on Florida Keys 11 years after the 1997/1998 El Niño. Mar Ecol Prog Ser 489:125–141CrossRefGoogle Scholar
  56. Sánchez JA (2009) Systematics of the candelabrum gorgonian corals (Eunicea Lamouroux; Plexauridae; Octocorallia; Cnidaria). Zool J Linn Soc 157:237–263CrossRefGoogle Scholar
  57. Sánchez J, Zea S, Díaz J (1998) Patterns of octocoral and black coral distribution in the oceanic barrier reef-complex of Providencia Island, Southwestern Caribbean. Caribb J Sci 34:250–264Google Scholar
  58. Sánchez JA, Gómez CE, Escobar D, Dueñas LF (2011) Diversidad, abundancia y amenazas de los octocorales de la Isla Malpelo, Pacífico Oriental Tropical, Colombia. Bol Invest Mar Cost 40:139–154Google Scholar
  59. Schuhmacher H (1997) Soft corals as reef builders. Proc 8th Int Coral Reef Symp 1:499–502Google Scholar
  60. Siegenthaler U, Stocker TF, Monnin E, Lüthi D, Schwander J, Stauffer B, Raynaud D, Barnola J-M, Fischer H, Masson-Delmotte V, Jouzel J (2005) Stable carbon cycle–climate relationship during the late Pleistocene. Science 310:1313–1317CrossRefPubMedGoogle Scholar
  61. Tambutté E, Tambutté S, Segonds N, Zoccola D, Venn A, Erez J (2011) Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification. Proc R Soc B 279:19–27CrossRefPubMedCentralPubMedGoogle Scholar
  62. Velimirov B, Böhm E (1976) Calcium and magnesium carbonate concentrations in different growth regions of gorgonians. Mar Biol 35:269–275CrossRefGoogle Scholar
  63. Velimirov B, King J (1979) Calcium uptake and net calcification rates in the octocoral Eunicella papillosa. Mar Biol 50:349–358CrossRefGoogle Scholar
  64. Venn AA, Tambutté E, Holcomb M, Laurenta J, Allemand D, Tambutté S (2013) Impact of seawater acidification on pH at the tissue–skeleton interface and calcification in reef corals. Proc Natl Acad Sci USA 110:1634–1639CrossRefPubMedCentralPubMedGoogle Scholar
  65. Villamizar E, Díaz MíC, Rutzler K, Nobrega RD (2013) Biodiversity, ecological structure, and change in the sponge community of different geomorphological zones of the barrier forereef at Carrie Bow Cay, Belize. Mar Ecol. doi: 10.1111/maec.12099
  66. Weinbauer M, Velimirov B (1995) Calcium, magnesium and strontium concentrations in the calcite sclerites of Mediterranean gorgonians (Coelenterata: Octocorallia). Estuar Coast Shelf Sci 40:87–104CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • C. E. Gómez
    • 1
    • 2
    • 4
  • V. J. Paul
    • 2
  • R. Ritson-Williams
    • 2
  • N. Muehllehner
    • 3
  • C. Langdon
    • 3
  • J. A. Sánchez
    • 1
    Email author
  1. 1.Laboratorio de Biología Molecular Marina-BIOMMAR, Departamento de Ciencias Biológicas, Facultad de CienciasUniversidad de los AndesBogotáColombia
  2. 2.Smithsonian Marine Station at Fort PierceFort PierceUSA
  3. 3.Marine Biology and Ecology, Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA
  4. 4.Department of BiologyTemple UniversityPhiladelphiaUSA

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