Abstract
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.
References
Agegian C (1985) The biogeochemical ecology of Porolithon gardineri (Foslie). Ph.D thesis, University of Hawaii, p 178
Allemand D, Bénazet-Tambutté S (1996) Dynamics of calcification in the Mediterranean red coral Corallium rubrum (Linnaeus) (Cnidaria, Octocorallia). J Exp Zool 276:270–278
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 13:237–264
Bayer F (1961) The shallow water octocorallia of the West Indian region: a manual for marine biologist. Martinus Nijhoff, The Hague, p 373
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 19:1897–1908
Caldeira K, Wickett M (2003) Anthropogenic carbon and ocean pH. Nature 425:365
Cary LR (1918) The gorgonacea as a factor in the formation of coral reefs. Carnegie Inst Wash Publications 213:341–362
Chan NCS, Connolly SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Global Change Biol 19:282–290
Chave K, Deffeyes K, Weyl P, Garrels R, Thompson M (1962) Observations on the solubility of skeletal carbonates in aqueous solutions. Science 137:33–34
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 151–187
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 280:20122374
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 110:11044–11049
Davies SP (1989) Short-term growth measurement of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395
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 22:113–127
Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res 34:1733–1743
Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication 3:191
Doney SC (2010) The growing human footprint on coastal and open-ocean biogeochemistry. Science 328:1512–1516
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 373:285–294
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 1:165–169
Gabay Y, Benayahu Y, Fine M (2013) Does elevated pCO2 affect reef octocorals? Ecol Evol 3:465–473
Gabay Y, Fine M, Barkay Z, Benayahu Y (2014) Octocoral tissue provides protection from declining oceanic pH. PLoS One 9(4):e91553
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 16:2388–2398
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 117:129–132
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 18:37–46
Goh NK, Peter KL, Chou L (1999) Notes on the shallow water gorgonian-associated fauna on coral reefs in Singapore. Bull Mar Sci 655:259–282
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 40:287–303
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 49:287–294
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 318:1737–1742
Inoue S, Kayanne H, Yamamoto S, Kurihara H (2013) Spatial community shift from hard to soft corals in acidified water. Nat Climate Change 3:683–687
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 1552
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 30:925–933
Jokiel P, Rodgers K, Kuffner I, Andersson A, Cox E, Mackenzie F (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27:473–483
Kingsley R, Watabe N (1989) The dynamics of spicule calcification in whole colonies of the gorgonian Leptogorgia virgulata. J Exp Mar Biol Ecol 133:57–65
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 284:118–120
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 74:4988–5001
Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434
Kuffner I, Andersson A, Jokiel P, Rodgers K, Mackenzie F (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1:114–117
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 164:513–531
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:C09S07
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 44:767–774
Lewis JC, Von Wallis E (1991) The function of surface sclerites in gorgonians (Coelenterata, Octocorallia). Biol Bull 181:275–288
Lucas J, Knapp L (1997) A physiological evaluation of carbon sources for calcification in the octocoral Leptogorgia virgulata (Lamarck). J Exp Biol 200:2653–2662
Manzello DP (2010) Coral growth with thermal stress and ocean acidification: lessons from the eastern tropical Pacific. Coral Reefs 29:749–758
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 23:423–432
Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Global Change Biol 15:2089–2100
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 18:897–907
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):e85557
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 70:5814–5830
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 202:175–192
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, TN
Purcell S, Blockmans B (2009) Effective fluorochrome marking of juvenile sea cucumbers for sea ranching and restocking. Aquaculture 296:263–270
Ries J, Cohen A, McCorkle D (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134
Ries J, Cohen A, McCorkle D (2010) A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. Coral Reefs 29:661–674
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 1:308–312
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 489:125–141
Sánchez JA (2009) Systematics of the candelabrum gorgonian corals (Eunicea Lamouroux; Plexauridae; Octocorallia; Cnidaria). Zool J Linn Soc 157:237–263
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 34:250–264
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 40:139–154
Schuhmacher H (1997) Soft corals as reef builders. Proc 8th Int Coral Reef Symp 1:499–502
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 310:1313–1317
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 279:19–27
Velimirov B, Böhm E (1976) Calcium and magnesium carbonate concentrations in different growth regions of gorgonians. Mar Biol 35:269–275
Velimirov B, King J (1979) Calcium uptake and net calcification rates in the octocoral Eunicella papillosa. Mar Biol 50:349–358
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 110:1634–1639
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
Weinbauer M, Velimirov B (1995) Calcium, magnesium and strontium concentrations in the calcite sclerites of Mediterranean gorgonians (Coelenterata: Octocorallia). Estuar Coast Shelf Sci 40:87–104
Acknowledgments
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Handling Editor Simon Davy
Rights and permissions
About this article
Cite this article
Gómez, C.E., Paul, V.J., Ritson-Williams, R. et al. Responses of the tropical gorgonian coral Eunicea fusca to ocean acidification conditions. Coral Reefs 34, 451–460 (2015). https://doi.org/10.1007/s00338-014-1241-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-014-1241-3