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Cold-Water Corals in an Era of Rapid Global Change: Are These the Deep Ocean’s Most Vulnerable Ecosystems?

Chapter

Abstract

Cold-water corals create highly complex biogenic habitats that promote and sustain high biological diversity in the deep sea and play critical roles in deep-water ecosystem functioning across the globe. However, these often out of sight and out of mind ecosystems are increasingly under pressure both from human activities in the deep sea such as fishing and mineral extraction, and from a rapidly changing climate. This chapter gives an overview of the importance of cold-water coral habitats, the threats they face and how recent advances in understanding of both past and present cold-water coral ecosystems helps us to understand how well they may be able to adapt to current and future climate change. We address key knowledge gaps and the ongoing efforts at national and international scales to promote and protect these important yet vulnerable ecosystems.

Keywords

Cold-water coral Ocean acidification Aragonite saturation horizon Lophelia pertusa Conservation 

References

  1. Adkins JF, Boyle EA, Curry WB, Lutringer A (2003) Stable isotopes in deep-sea corals and a new mechanism for “vital effects”. Geochim Cosmochim Acta 67(6):1129–1143CrossRefGoogle Scholar
  2. Albright R, Mason B (2013) Projected near-future levels of temperature and pCO2 reduce coral fertilization success. PLoS ONE 8(2):e56468CrossRefPubMedPubMedCentralGoogle Scholar
  3. Al-Horani FA, Al-Moghrabi SM, de Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142(3):419–426Google Scholar
  4. Althaus F, Williams A, Schlacher TA, Kloser RJ, Green MA, Barker BA, Bax NJ, Brodie P, Hoenlinger-Schlacher MA (2009) Impacts of bottom trawling on deep-coral ecosystems of seamounts are long-lasting. Mar Ecol Prog Ser 397:279–294CrossRefGoogle Scholar
  5. Anagnostou E, Sherrell RM, Gagnon A, LaVigne M, Field MP, McDonough WF (2011) Seawater nutrient and carbonate ion concentrations recorded as P/Ca, Ba/Ca, and U/Ca in the deep-sea coral Desmophyllum dianthus. Geochim Cosmochim Acta 75(9):2529–2543CrossRefGoogle Scholar
  6. Anagnostou E, Huang KF, You CF, Sikes EL, Sherrell RM (2012) Evaluation of boron isotope ratio as a pH proxy in the deep sea coral Desmophyllum dianthus: evidence of physiological pH adjustment. Earth Planet Sci Lett 349:251–260CrossRefGoogle Scholar
  7. Armstrong CW, van den Hove S (2008) The formation of policy for protection of cold-water coral off the coast of Norway. Mar Policy 32:66–73CrossRefGoogle Scholar
  8. Blamart D, Rollion-Bard C, Meibom A, Cuif JP, Juillet-Leclerc A, Dauphin Y (2007) Correlation of boron isotopic composition with ultrastructure in the deep-sea coral Lophelia pertusa: implications for biomineralization and paleo-pH. Geochem Geophys Geosyst 8(12). doi: 10.1029/2007gc001686 Google Scholar
  9. Buhl-Mortensen L, Mortensen PB (2004) Symbiosis in deep-water corals. Symbiosis 37:33–61Google Scholar
  10. Cairns SD (2007) Deep-water corals: an overview with special reference to diversity and distribution of deep-water scleractinian corals. Bull Mar Sci 81:311–322Google Scholar
  11. Cairns SD (2011) Global diversity of the Stylasteridae (Cnidaria: Hydrozoa: Athecatae). PLoS ONE 6(7):e21670CrossRefPubMedPubMedCentralGoogle Scholar
  12. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefPubMedGoogle Scholar
  13. Carreiro-Silva M, Cerqueira T, Godinho A, Caetano M, Santos RS, Bettencourt R (2014) Molecular mechanisms underlying the physiological responses of the cold-water coral Desmophyllum dianthus to ocean acidification. Coral Reefs 33(2):465–476CrossRefGoogle Scholar
  14. Case DH, Robinson LF, Auro ME, Gagnon AC (2010) Environmental and biological controls on Mg and Li in deep-sea scleractinian corals. Earth Planet Sci Lett 300(3–4):215–225CrossRefGoogle Scholar
  15. Cathalot C, Van Oevelen D, Cox TJS, Kutti T, Lavaleye M, Duineveld G, Meysman FJR (2015) Cold-water coral reefs and adjacent sponge grounds: hotspots of benthic respiration and organic carbon cycling in the deep sea. Front Mar Sci 2:37. doi: 10.3389/fmars.2015.00037 CrossRefGoogle Scholar
  16. CBD (2008) Synthesis and review of the best available scientific studies on priority areas for biodiversity conservation in marine areas beyond the limits of national jurisdiction. Montreal, Technical Series No. 37, 63 pagesGoogle Scholar
  17. CBD (2014a) An updated synthesis on the impacts of ocean acidification on marine biodiversity. Technical Series No. 75. MontrealGoogle Scholar
  18. CBD (2014b) Global biodiversity outlook 4. Convention on Biological Diversity, Montréal, p 155Google Scholar
  19. Cheng H, Adkins J, Edwards RL, Boyle EA (2000) U-Th dating of deep-sea corals. Geochim Cosmochim Acta 64(14):2401–2416CrossRefGoogle Scholar
  20. Cheng W, Chiang JCH, Zhang D (2013) Atlantic Meridional Overturning Circulation (AMOC) in CMIP5 models: RCP and historical simulations. J Clim 26(18):7187–7197CrossRefGoogle Scholar
  21. Cohen AL, McConnaughey TA (2003) Geochemical perspectives on coral mineralization. In: Dove PM, De Yoreo J, Weiner S (eds) Biomineralization, vol 54, Reviews in mineralogy and geochemistry. Mineralogical Society of America, Washington, DC, pp 151–187Google Scholar
  22. Cohen AL, McCorkle DC, de Putron S, Gaetani GA, Rose KA (2009) Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawater: insights into the biomineralization response to ocean acidification. Geochem Geophys Geosyst 10:Q07005, doi:Q0700510.1029/2009gc002411CrossRefGoogle Scholar
  23. Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2013) The responses of eight coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping point. Limnol Oceanogr 58(1):388–398CrossRefGoogle Scholar
  24. Corell H, Moksnes PO, Engqvist A, Döös K, Jonsson PR (2012) Depth distribution of larvae critically affects their dispersal and the efficiency of marine protected areas. Mar Ecol Prog Ser 467:29–46CrossRefGoogle Scholar
  25. Coscia I, Robins PE, Porter JS, Malham SK, Ironside JE (2012) Modelled larval dispersal and measured gene flow: seascape genetics of the common cockle Cerastoderma edule in the southern Irish Sea. Conserv Genet 14(2):451–466CrossRefGoogle Scholar
  26. Dahl M (2013) Conservation genetics of Lophelia pertusa. PhD thesis, University of GothenbergGoogle Scholar
  27. Davies AJ, Duineveld GCA, Lavaleye MSS, Bergman MIN, van Haren H, Roberts JM (2009) Downwelling and deep-water bottom currents as food supply mechanisms to the cold-water Lophelia pertusa (Scleractinia) at the Mingulay Reef complex. Limnol Oceanogr 54(2):620–629CrossRefGoogle Scholar
  28. Dodds LA, Roberts JM, Taylor AC, Marubini F (2007) Metabolic tolerance of the cold-water coral Lophelia pertusa (Scleractinia) to temperature and dissolved oxygen change. J Exp Mar Biol Ecol 349(2):205–214CrossRefGoogle Scholar
  29. Dodds LA, Black KD, Orr H, Roberts JM (2009) Lipid biomarkers reveal geographic differences in food supply to the cold-water coral Lophelia pertusa (Scleractinia). Mar Ecol Prog Ser 397:113–124CrossRefGoogle Scholar
  30. Douville E, Salle E, Frank N, Eisele M, Pons-Branchu E, Ayrault S (2010) Rapid and accurate U-Th dating of ancient carbonates using inductively coupled plasma-quadrupole mass spectrometry. Chem Geol 272(1–4):1–11CrossRefGoogle Scholar
  31. Duineveld GCA, Lavaleye MSS, Berghuis EM (2004) Particle flux and food supply to a seamount cold-water coral community (Galicia Bank, NW Spain). Mar Ecol Prog Ser 277:13–23CrossRefGoogle Scholar
  32. Duineveld GCA, Lavaleye MSS, Bergman MJN, de Stigter H, Mienis F (2007) Trophic structure of a cold-water coral mound community (Rockall Bank, NE Atlantic) in relation to the near-bottom particle supply and current regime. Bull Mar Sci 81(3):449–467Google Scholar
  33. EC (1992) Council directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and floraGoogle Scholar
  34. Eyre BD, Andersson AJ, Cyronak T (2014) Benthic coral reef calcium carbonate dissolution in an acidifying ocean. Nat Clim Chang 4(11):969–976CrossRefGoogle Scholar
  35. FAO (2009) Deep-sea fisheries in the high seas. Ensuring sustainable use of marine resources and the protection of vulnerable marine ecosystems. Food and Agriculture Organization of the United Nations, Rome, 11ppGoogle Scholar
  36. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305(5682):362–366CrossRefPubMedGoogle Scholar
  37. Fillinger L, Richter C (2013) Vertical and horizontal distribution of Desmophyllum dianthus in Comau Fjord, Chile: a cold-water coral thriving at low pH. Peer J 1:e194CrossRefPubMedPubMedCentralGoogle Scholar
  38. Flot JF, Dahl M, André C (2013) Lophelia pertusa corals from the Ionian and Barents seas share identical nuclear ITS2 and near-identical mitochondrial genome sequences. BMC Res Notes 6(1):144CrossRefPubMedPubMedCentralGoogle Scholar
  39. Form AU, Riebesell U (2012) Acclimation to ocean acidification during long-term CO2 exposure in the cold-water coral Lophelia pertusa. Glob Chang Biol 18(3):843–853CrossRefGoogle Scholar
  40. Frieler K, Meinshausen M, Golly A, Mengel M, Lebek K, Donner SD, Hoegh-Guldberg O (2013) Limiting global warming to 2 °C is unlikely to save most coral reefs. Nat Clim Chang 3(2):165–170CrossRefGoogle Scholar
  41. Gagnon AC (2013) Coral calcification feels the acid. Proc Natl Acad Sci U S A 110(5):1567–1568CrossRefPubMedPubMedCentralGoogle Scholar
  42. Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39(1):30–43CrossRefGoogle Scholar
  43. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21(3):394–407CrossRefGoogle Scholar
  44. Gillett NP, Arora VK, Matthews D, Allen MR (2013) Constraining the ratio of global warming to cumulative CO2 emissions using CMIP5 simulations. J Clim 26(18):6844–6858CrossRefGoogle Scholar
  45. Gradstein FM, Ogg JG, Smith AG (2004) A geologic time scale. Cambridge University Press, CambridgeGoogle Scholar
  46. Guinotte JM, Orr J, Cairns S, Freiwald A, Morgan L, George R (2006) Will human-induced changes in seawater chemistry alter the distribution of deep-sea scleractinian corals? Front Ecol Environ 4(3):141–146CrossRefGoogle Scholar
  47. Hebbeln D, Wienberg C, Wintersteller P, Freiwald A, Becker M, Beuck L, Dullo C, Eberli GP, Glogowski S, Matos L, Forster N, Reyes-Bonilla H, Taviani M (2014) Environmental forcing of the Campeche cold-water coral province, southern Gulf of Mexico. Biogeosciences 11(7):1799–1815CrossRefGoogle Scholar
  48. Hennige S, Wicks LC, Keamenos N, Bakker DCE, Findlay HS, Dumousseaud C, Roberts JM (2014a) Short term metabolic and growth responses of the cold-water coral Lophelia pertusa to ocean acidification. Deep Sea Res II 99:27–35CrossRefGoogle Scholar
  49. Hennige SJ, Morrison CL, Form A, Buscher J, Kamenos NA, Roberts JM (2014b) Self recognition in corals facilitates deep-sea habitat engineering. Sci Rep 4:6782CrossRefPubMedGoogle Scholar
  50. Hennige SJ, Wicks LC, Kamenos NA, Perna G, Findlay HS, Roberts JM (2015) Hidden impacts of ocean acidification to live and dead coral framework. Proc R Soc B Biol Sci 282:20150990CrossRefGoogle Scholar
  51. Henry LA, Vad J, Findlay HS, Murillo J, Milligan R, Roberts JM (2014a) Environmental variability and biodiversity of megabenthos on the Hebrides Terrace Seamount (Northeast Atlantic). Sci Rep 4:5589CrossRefPubMedPubMedCentralGoogle Scholar
  52. Henry LA, Frank N, Hebbeln D, Wienberg C, Robinson L, van de Flierdt T, Dahl M, Douarin M, Morrison CL, López Correa M, Rogers AD, Ruckelshausen M, Roberts JM (2014b) Global ocean conveyor lowers extinction risk in the deep sea. Deep-Sea Res I 88:8–16Google Scholar
  53. IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge. doi: 10.1017/CBO9781107415324, 1535 ppGoogle Scholar
  54. Jantzen C, Haussermann V, Forsterra G, Laudien J, Ardelan M, Maier S, Richter C (2013) Occurrence of a cold-water coral along natural pH gradients (Patagonia, Chile). Mar Biol 160(10):2597–2607CrossRefGoogle Scholar
  55. Jump AS, Penuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett 8(9):1010–1020CrossRefGoogle Scholar
  56. Kiriakoulakis K, Bett BJ, White M, Wolff GA (2004) Organic biogeochemistry of the Darwin Mounds, a deep-water coral ecosystem, of the NE Atlantic. Deep Sea Res Part I Oceanogr Res Pap 51(12):1937–1954CrossRefGoogle Scholar
  57. Klochko K, Kaufman AJ, Yao W, Byrne RH, Tossell JA (2006) Experimental measurement of boron isotope fractionation in seawater. Earth Planet Sci Lett 248(1–2):276–285CrossRefGoogle Scholar
  58. Knoll AH, Bambach RK, Canfield DE, Grotzinger JP (1996) Comparative earth history and late Permian mass extinction. Science 273:452–457CrossRefGoogle Scholar
  59. Langdon C, Takahashi T, Sweeney C, Chipman D, Goddard J, Marubini F, Aceves H, Barnett H, Atkinson MJ (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Glob Biogeochem Cycles 14(2):639–654CrossRefGoogle Scholar
  60. Larsson AI, Jarnegren J, Stromberg SM, Dahl MP, Lundalv T, Brooke S (2014) Embryogenesis and larval biology of the cold-water coral Lophelia pertusa. PLoS ONE 9(7):14CrossRefGoogle Scholar
  61. Lomitschka M, Mangini A (1999) Precise Th/U dating of small and heavily coated samples of deep sea corals. Earth Planet Sci Lett 170:391–401CrossRefGoogle Scholar
  62. Longworth BE, Robinson LF, Roberts ML, Beaupre SR, Burke A, Jenkins WJ (2013) Carbonate as sputter target material for rapid 14C AMS. Nucl Inst Methods Phys Res Sect B Beam Interact Mater Atom 294:328–334CrossRefGoogle Scholar
  63. Lunden JJ, McNicholl CG, Sears CR, Morrison CL, Cordes EE (2014) Acute survivorship of the deep-sea coral Lophelia pertusa from the Gulf of Mexico under acidification, warming, and deoxygenation. Front Mar Sci 1:78CrossRefGoogle Scholar
  64. Maier C, Hegeman J, Weinbauer MG (2009) Calcification of the cold-water coral Lophelia pertusa under ambient and reduced pH. Biogeosciences 6:1671–1680CrossRefGoogle Scholar
  65. Maier C, Bils F, Weinbauer MG, Watremez P, Peck MA, Gattuso JP (2013a) Respiration of Mediterranean cold-water corals is not affected by ocean acidification as projected for the end of the century. Biogeosciences 10:5671–5680CrossRefGoogle Scholar
  66. Maier C, Schubert A, Sanchez MMB, Weinbauer MG, Watremez P, Gattuso J-P (2013b) End of the century pCO2 levels do not impact calcification in Mediterranean cold-water corals. PLoS ONE 8(4):e62655CrossRefPubMedPubMedCentralGoogle Scholar
  67. Mason HE, Montagna P, Kubista L, Taviani M, McCulloch M, Phillips BL (2011) Phosphate defects and apatite inclusions in coral skeletal aragonite revealed by solid-state NMR spectroscopy. Geochim Cosmochim Acta 75(23):7446–7457CrossRefGoogle Scholar
  68. McConnaughey T (1989) 13C and 18O isotopic disequilibrium in biological carbonates. I. Patterns. Geochim Cosmochim Acta 53(1):151–162CrossRefGoogle Scholar
  69. McCulloch M, Falter J, Trotter J, Montagna P (2012a) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2(8):623–633CrossRefGoogle Scholar
  70. McCulloch M, Trotter J, Montagna P, Falter J, Dunbar R, Freiwald A, Foersterra N, Lopez Correa M, Maier C, Ruggeberg A, Taviani M (2012b) Resilience of cold-water scleractinian corals to ocean acidification: boron isotopic systematics of pH and saturation state up-regulation. Geochim Cosmochim Acta 87:21–34CrossRefGoogle Scholar
  71. McIntyre CP, Roberts ML, Burton JR, McNichol AP, Burke A, Robinson LF, von Reden KF, Jenkins WJ (2011) Rapid radiocarbon (14C) analysis of coral and carbonate samples using a continuous-flow accelerator mass spectrometry (CFAMS) system. Paleoceanography 26(4). doi: 10.1029/2011pa002174
  72. Miller KJ, Rowden AA, Williams A, Haussermann V (2011) Out of their depth? Isolated deep populations of the cosmopolitan coral Desmophyllum dianthus may be highly vulnerable to environmental change. PLoS ONE 6(5):e19004CrossRefPubMedPubMedCentralGoogle Scholar
  73. Montagna P, McCulloch M, Taviani M, Mazzoli C, Vendrell B (2006) Phosphorus in cold-water corals as a proxy for seawater nutrient chemistry. Science 312:1788–1791CrossRefPubMedGoogle Scholar
  74. Montagna P, McCulloch M, Douville E, López Correa M, Trotter J, Rodolfo-Metalpa R, Dissard D, Ferrier-Pagès C, Frank N, Freiwald A, Goldstein S, Mazzoli C, Reynaud S, Rüggeberg A, Russo S, Taviani M (2014) Li/Mg systematics in scleractinian corals: calibration of the thermometer. Geochim Cosmochim Acta 132:288–310CrossRefGoogle Scholar
  75. Morrison CL, Ross SW, Nizinski MS, Brooke S, Järnegren J, Waller RG, Johnson RL, King TL (2011) Genetic discontinuity among regional populations of Lophelia pertusa in the North Atlantic Ocean. Conserv Genet 12(3):713–729CrossRefGoogle Scholar
  76. Movilla J, Gori A, Calvo E, Orejas C, Lopez-Sanz A, Dominguez-Carrio C, Grinyo J, Pelejero C (2014) Resistance of two Mediterranean cold-water coral species to low-pH conditions. Water 6(1):59–67CrossRefGoogle Scholar
  77. Naumann MS, Orejas C, Ferrier-Pagès C (2013) High thermal tolerance of two Mediterranean cold-water coral species maintained in aquaria. Coral Reefs 32(3):749–754CrossRefGoogle Scholar
  78. Nir O, Vengosh A, Harkness JS, Dwyer GS, Lahav O (2015) Direct measurement of the boron isotope fractionation factor: reducing the uncertainty in reconstructing ocean paleo-pH. Earth Planet Sci Lett 414:1–5CrossRefGoogle Scholar
  79. O’Leary BC, Brown RL, Johnson DE, Von Nordheim H, Ardron J, Packeiser T, Roberts CM (2012) The first network of marine protected areas (MPAs) in the high seas: the process, the challenges and where next. Mar Policy 36(3):598–605CrossRefGoogle Scholar
  80. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437(7059):681–686CrossRefPubMedGoogle Scholar
  81. Palanques A, Martín J, Puig P, Guillén J, Company JB, Sardà F (2006) Evidence of sediment gravity flows induced by trawling in the Palamós (Fonera) submarine canyon (northwestern Mediterranean). Deep-Sea Res I Oceanogr Res Pap 53(2):201–214CrossRefGoogle Scholar
  82. Pfennig DW, Wund MA, Snell-Rood EC, Cruickshank T, Schlichting CD, Moczek AP (2010) Phenotypic plasticity’s impacts on diversification and speciation. Trends Ecol Evol 25(8):459–467CrossRefPubMedGoogle Scholar
  83. Pinto JG, Ulbrich U, Leckebusch GC, Spangehl T, Reyers M, Zacharias S (2007) Changes in storm track and cyclone activity in three SRES ensemble experiments with the ECHAM5/MPI-OM1 GCM. Clim Dyn 29(2–3):195–210CrossRefGoogle Scholar
  84. Ramirez-Llodra E, Tyler PA, Baker MC, Bergstad OA, Clark MR, Elva Escobar E, Levin LA, Menot L, Rowden AA, Smith CR, Van Dover CL (2011) Man and the last great wilderness: human impact on the deep sea. PLoS ONE 6(8):e22588CrossRefPubMedPubMedCentralGoogle Scholar
  85. Reed TE, Schindler DE, Waples RS (2011) Interacting effects of phenotypic plasticity and evolution on population persistence in a changing climate. Conserv Biol J Soc Conserv Biol 25(1):56–63CrossRefGoogle Scholar
  86. Revelle R, Suess HE (1957) Carbon dioxide exchange between atmosphere and ocean and the question of an increase of atmospheric CO2 during the past decades. Tellus 9(1):18–27CrossRefGoogle Scholar
  87. Roberts JM (2005) Reef-aggregating behavior by symbiotic eunicid polychaetes from cold-water corals: do worms assemble reefs? J Mar Biol Assoc U K 85:813–819CrossRefGoogle Scholar
  88. Roberts JM, Shipboard Party (2013) Changing oceans expedition 2012. RRS James Cook 073 cruise report. Heriot-Watt University, Edinburgh, UK, 224 ppGoogle Scholar
  89. Roberts JM, Wheeler AJ, Freiwald A (2006) Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312(5773):543–547CrossRefPubMedGoogle Scholar
  90. Roberts JM, Wheeler A, Freiwald A, Cairns SD (2009) Cold-water corals: the biology and geology of deep-sea coral habitats. Cambridge University Press, Cambridge, Edinburgh, UK, 334ppGoogle Scholar
  91. Rodolfo-Metalpa R, Montagna P, Aliani S, Borghini M, Canese S, Hall-Spencer JM, Foggo A, Milazzo M, Taviani M, Houlbrèque F (2015) Calcification is not the Achilles’ heel of cold-water corals in an acidifying ocean. Glob Chang Biol. doi: 10.1111/gcb.12867 PubMedGoogle Scholar
  92. Rollion-Bard C, Erez J (2010) Intra-shell boron isotope ratios in the symbiont-bearing benthic foraminiferan Amphistegina lobifera: implications for δ11B vital effects and paleo-pH reconstructions. Geochim Cosmochim Acta 74(5):1530–1536CrossRefGoogle Scholar
  93. Rovelli L, Attard KM, Bryant LD, Flögel S, Stahl H, Roberts JM, Linke P, Glud RN (2015) Benthic O2 uptake of two cold-water coral communities estimated with the non-invasive eddy correlation technique. Mar Ecol Prog Ser 525:97–104CrossRefGoogle Scholar
  94. Silbiger NJ, Donahue MJ (2015) Secondary calcification and dissolution respond differently to future ocean conditions. Biogeosciences 12:567–578CrossRefGoogle Scholar
  95. Stanley GD Jr (2003) The evolution of modern corals and their early history. Earth Sci Rev 60(3–4):195–225CrossRefGoogle Scholar
  96. Stern N, Taylor C (2010) What do the appendices to the Copenhagen accord tell us about global greenhouse gas emissions and the prospects for avoiding a rise in global average temperature of more than 2°C? Policy Paper, Centre for Climate Change Economics and Policy, p 26Google Scholar
  97. Stone RP (2014) The ecology of deep-sea coral and sponge habitats of the central Aleutian Islands of Alaska. NOAA Prof Pap NMFS 16:1–52Google Scholar
  98. Tambutté S, Holcomb M, Ferrier-Pagès C, Reynaud S, Tambutté É, Zoccola D, Allemand D (2011) Coral biomineralization: from the gene to the environment. J Exp Mar Biol Ecol 408(1–2):58–78CrossRefGoogle Scholar
  99. Thiagarajan N, Adkins J, Eiler J (2011) Carbonate clumped isotope thermometry of deep-sea corals and implications for vital effects. Geochim Cosmochim Acta 75(16):4416–4425CrossRefGoogle Scholar
  100. Thiagarajan N, Gerlach D, Roberts ML, Burke A, McNichol A, Jenkins WJ, Subhas AV, Thresher RE, Adkins JF (2013) Movement of deep-sea coral populations on climatic timescales. Paleoceanography 28(2):227–236CrossRefGoogle Scholar
  101. Thresher RE, Tilbrook B, Fallon S, Wilson NC, Adkins J (2011) Effects of chronic low carbonate saturation levels on the distribution, growth and skeletal chemistry of deep-sea corals and other seamount megabenthos. Mar Ecol Prog Ser 442:87–99CrossRefGoogle Scholar
  102. Venn A, Tambutté E, Lotto S,D (2009) Imaging intracellular pH in a reef coral and symbiotic anemone. Proc Natl Acad Sci 106(39):16574–16579CrossRefPubMedPubMedCentralGoogle Scholar
  103. Venn A, Tambutte E, Holcomb M, Allemand D, Tambutte S (2011) Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS ONE 6(5):e20013CrossRefPubMedPubMedCentralGoogle Scholar
  104. Venn AA, Tambutte E, Holcomb M, Laurent J, Allemand D, Tambutte S (2013) Impact of seawater acidification on pH at the tissue-skeleton interface and calcification in reef corals. Proc Natl Acad Sci U S A 110(5):1634–1639CrossRefPubMedGoogle Scholar
  105. Veron JEN (2008) Mass extinctions and ocean acidification: biological constraints on geological dilemmas. Coral Reefs 27(3):459–472CrossRefGoogle Scholar
  106. Wicks LC, Roberts JM (2012) Benthic invertebrates in a high-CO2 world. Oceanogr Mar Biol Annu Rev 50:127–188CrossRefGoogle Scholar
  107. Widdicombe S, Spicer JI (2008) Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us? J Exp Mar Biol Ecol 366(1–2):187–197CrossRefGoogle Scholar
  108. Wisshak M, Schoenberg CHL, Form A, Freiwald A (2012) Ocean acidification accelerates reef bioerosion. PLoS ONE 7(9):e45124CrossRefPubMedPubMedCentralGoogle Scholar
  109. Zeebe RE, Wolf-Gladrow D (2005) CO2 in seawater: equilibrium, kinetics, isotopes. Elsevier, AmsterdamGoogle Scholar
  110. Zoccola D, Tambutte E, Kulhanek E, Puverel S, Scimeca JC, Allemand D, Tambutte S (2004) Molecular cloning and localization of a PMCA P-type calcium ATPase from the coral Stylophora pistillata. Biochim Biophys Acta 1663(1–2):117–126CrossRefPubMedGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Centre for Marine Biodiversity & BiotechnologyHeriot-Watt UniversityEdinburghUK
  2. 2.Ocean and Earth Science, National Oceanography Centre SouthamptonUniversity of SouthamptonSouthamptonUK
  3. 3.Departament d’EcologiaUniversitat de BarcelonaBarcelonaSpain
  4. 4.School of Geographical and Earth Sciences, Gregory BuildingUniversity of GlasgowGlasgowUK

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