Physiological performance of the cold-water coral Dendrophyllia cornigera reveals its preference for temperate environments

Abstract

Cold-water corals (CWCs) are key ecosystem engineers in deep-sea benthic communities around the world. Their distribution patterns are related to several abiotic and biotic factors, of which seawater temperature is arguably one of the most important due to its role in coral physiological processes. The CWC Dendrophyllia cornigera has the particular ability to thrive in several locations in which temperatures range from 11 to 17 °C, but to be apparently absent from most CWC reefs at temperatures constantly below 11 °C. This study thus aimed to assess the thermal tolerance of this CWC species, collected in the Mediterranean Sea at 12 °C, and grown at the three relevant temperatures of 8, 12, and 16 °C. This species displayed thermal tolerance to the large range of seawater temperatures investigated, but growth, calcification, respiration, and total organic carbon (TOC) fluxes severely decreased at 8 °C compared to the in situ temperature of 12 °C. Conversely, no significant differences in calcification, respiration, and TOC fluxes were observed between corals maintained at 12 and 16 °C, suggesting that the fitness of this CWC is higher in temperate rather than cold environments. The capacity to maintain physiological functions between 12 and 16 °C allows D. cornigera to be the most abundant CWC species in deep-sea ecosystems where temperatures are too warm for other CWC species (e.g., Canary Islands). This study also shows that not all CWC species occurring in the Mediterranean Sea (at deep-water temperatures of 12–14 °C) are currently living at their upper thermal tolerance limit.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Abramovitch-Gottlib L, Katoshevski D, Vago R (2002) A computerized tank system for studying the effect of temperature on calcification of reef organisms. J Biochem Biophys Methods 50:245–252

    CAS  PubMed  Article  Google Scholar 

  2. Al-Horani FA (2005) Effects of changing seawater temperature on photosynthesis and calcification in the scleractinian coral Galaxea fascicularis, measured with O2, Ca2+ and pH microsensors. Sci Mar 69:347–354

    CAS  Article  Google 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 142:419–426

    CAS  Google Scholar 

  4. Allemand D, Ferrier-Pagès C, Furla P, Houlbrèque F, Puverel S, Reynaud S, Tambutté E, Tambutté S, Zoccola D (2004) Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. C R Palevol 3:453–467

    Article  Google Scholar 

  5. Álvarez-Claudio C (1994) Deep-water Scleractinia (Cnidaria Anthozoa) from southern Biscay Bay. Cah Biol Mar 35:461–469

    Google Scholar 

  6. Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energy budgets at variable turbidity. J Exp Mar Biol Ecol 252:221–253

    PubMed  Article  Google Scholar 

  7. Baillon S, Hamel JF, Wareham VE, Mercier A (2012) Deep cold-water corals as nurseries for fish larvae. Front Ecol Environ 10:351–356

    Article  Google Scholar 

  8. Barton ED, Arístegui J, Tett P, Cantón M, García-Braun J, Hernández-León S, Nykjaer L, Almeida C, Almunia J, Ballesteros S, Basterretxea G, Escánez J, García-Weill L, Hernández-Guerra A, López-Laatzen F, Molina R, Montero MF, Navarro-Pérez E, Rodríguez JM, van Lenning K, Vélez H, Wild K (1998) The transition zone of the Canary Current upwelling region. Prog Oceanogr 41:450–455

    Article  Google Scholar 

  9. Bethoux JP, Gentili B, Raunet J, Tailliez D (1990) Warming trend in the western Mediterranean deep water. Nature 347:660–662

    Article  Google Scholar 

  10. Bo M, Bertolino B, Borghini M, Castellano M, Harriague AC, Di Camillo CG, Gasparini G, Misic C, Povero P, Pusceddu A, Schroeder K, Bavestrello G (2011) Characteristics of the mesophotic megabenthic assemblages of the Vercelli Seamount (North Tyrrhenian Sea). PLoS One 6:e16357

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  11. Braga-Henriques A, Porteiro FM, Ribeiro PA, de Matos V, Sampaio Í, Ocaña O, Santos RS (2013) Diversity, distribution and spatial structure of the cold-water coral fauna of the Azores (NE Atlantic). Biogeosciences 10:4009–4036

    Article  Google Scholar 

  12. Brito A, Ocaña O (2004) Corales de las islas Canarias. Antozoos con esqueleto de los fondos litorales y profundos. Francisco Lemus Editor, La Laguna

  13. Brooke S, Ross SW, Bane JM, Seim HE, Young CM (2013) Temperature tolerance of the deep-sea coral Lophelia pertusa from the southeastern United States. Deep Sea Res Pt 2 Top Stud Oceanogr 92:240–248

  14. Buddemeier RW, Kinzie RA (1976) Coral growth. Oceanogr Mar Biol Annu Rev 14:183–225

    Google Scholar 

  15. Buhl-Mortensen LA, Vanreusel AJ, Gooday LA, Levin I, Priede G, Buhl-Mortensen P, Gheerardyn H, King NJ, Raes M (2010) Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Mar Ecol 31:21–50

    Article  Google Scholar 

  16. Cairns SD (1994) Scleractinia of the temperate north Pacific. Smithsonian Institution Press, Washington, DC, pp 1–150

    Google Scholar 

  17. Carlier A, Le Guilloux E, Olu K, Sarrazin J, Mastrototaro F, Taviani M, Clavier J (2009) Trophic relationships in a deep Mediterranean cold-water coral bank (Santa Maria di Leuca, Ionian Sea). Mar Ecol Prog Ser 397:125–137

    CAS  Article  Google Scholar 

  18. Caroselli E, Zaccanti F, Mattioli G, Falini G, Levy O, Dubinsky Z, Goffredo S (2012) Growth and demography of the solitary scleractinian coral Leptopsammia pruvoti along a sea surface temperature gradient in the Mediterranean Sea. PLoS One 76:e37848

    Article  Google Scholar 

  19. Carricart-Garnivet JP (2004) Sea surface temperature and the growth of the West Atlantic reef building coral Montastrea annularis. J Exp Mar Biol Ecol 302:249–260

    Article  Google Scholar 

  20. Castaing P, Froidefond JM, Lazure P, Weber O, Prud’homme R, Jouanneau JM (1999) Relationship between hydrology and seasonal distribution of suspended sediments on the continental shelf of the Bay of Biscay. Deep-Sea Res Part 2 Top Stud Oceanogr 46:1979–2001

  21. Castric-Fey A (1996) Le Scléractiniaire Dendrophyllia cornigera en eau peu profonde, à Ouessant (Bretagna, Atlantique NE) en l’absence de barrière thermique. Oceanologica Acta 19:665–671

    Google Scholar 

  22. Clausen CD, Roth AA (1975) Effect of temperature and temperature adaptation on calcification rate in the hermatypic coral Pocillopora damicornis. Mar Biol 33:93–100

    Article  Google Scholar 

  23. Colella MA, Ruzucka RR, Kidney JA, Morrison JM, Brinkhuis VB (2012) Cold-water event of January 2010 results in catastrophic benthic mortality on patch reefs in the Florida Keys. Coral Reefs 31:621–632

    Article  Google Scholar 

  24. Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol 43:209–216

    CAS  Article  Google Scholar 

  25. Coles SL, Jokiel PL (1978) Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Mar Biol 49:187–195

    Article  Google Scholar 

  26. Coles SL, Fadlallah YH (1991) Reef coral survival and mortality at low temperatures in the Arabian Gulf: new species-specific lower temperature limits. Coral Reefs 9:231–237

    Article  Google Scholar 

  27. Colombo-Pallotta MF, Rodriguez-Roman A, Iglesias-Prieto R (2010) Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29:899–907

    Article  Google Scholar 

  28. Crossland C (1987) In situ release of mucus and DOC-lipid from the corals Acropora variabilis and Stylophora pistillata in different light regimes. Coral Reefs 6:35–42

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  30. Davies AJ, Wisshak MO, James C, Roberts JM (2008) Predicting suitable habitat for the cold-water coral Lophelia pertusa (Scleractinia). Deep Sea Res Pt 1 Oceanogr Res Pap 55:1048–1062

  31. 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 349:205–214

    CAS  Article  Google Scholar 

  32. Dodds LA, Black KD, Orr H, Roberts JM (2009) Lipid biomarkers reveal geographical differences in food supply to the cold-water coral Lophelia pertusa (Scleractinia). Mar Ecol Prog Ser 397:113–124

    CAS  Article  Google Scholar 

  33. Duineveld G, Lavaleye M, Berghuis E (2004) Particle flux and food supply to a seamount cold-water coral community (Galicia Bank, NW Spain). Mar Ecol Prog Ser 277:13–23

    Article  Google Scholar 

  34. Duineveld G, Lavaleye M, Bergman M, 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 81:449–467

    Google Scholar 

  35. Duineveld GCA, Jeffreys RM, Lavaleye MSS, Davies AJ, Bergman MJN, Watmough T, Witbaard R (2012) Spatial and tidal variation in food supply to shallow cold-water coral reefs of the Mingulay Reef complex (Outer Hebrides, Scotland). Mar Ecol Prog Ser 444:97–115

    Article  Google Scholar 

  36. Dullo WC, Flögel S, Rüggeberg A (2008) Cold-water coral growth in relation to the hydrography of the Celtic and Nordic European continental margin. Mar Ecol Prog Ser 371:165–176

    Article  Google Scholar 

  37. Ferrier-Pagès C, Reynaud S, Allemand D (2012) Shallow water Scleractinian corals of the Mediterranean Sea. In: Stambler N (ed) Life in the Mediterranean Sea: a look at habitat changes. Nova Science Publishers Inc., New York

    Google Scholar 

  38. Ferrier-Pages C, Leclercq N, Jaubert J, Pelegri SP (2000) Enhancement of pico- and nanoplankton growth by coral exudates. Aquat Microb Ecol 21:203–209

    Article  Google Scholar 

  39. Ferrier-Pagès C, Gattuso JP, Cauwet G, Jaubert J, Allemand D (1998) Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis. Mar Ecol Prog Ser 172:265–274

    Article  Google Scholar 

  40. Fosså JH, Mortensen PB, Furevik DM (2002) The deepwater coral Lophelia pertusa in Norwegian waters: distribution and fishery impacts. Hydrobiologia 471:1–12

    Article  Google Scholar 

  41. Freiwald A, Fossa JH, Grehan A, Koslow T, Roberts JM (2004) Cold-water coral reefs-out of sight no longer our of mind. Biodiversity Series 22. UNEP-WCMC, Cambridge, UK

  42. Freiwald A, Beuck L, Rüggeberg A, Taviani M, Hebbeln D (2009) The white coral community in the Central Mediterranean Sea revealed by ROV surveys. Oceanography 22:58–74

    Article  Google Scholar 

  43. Gili JM, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Tree 13:316–321

    CAS  PubMed  Google Scholar 

  44. Glynn PW, Stewart RH (1973) Distribution of coral reefs in the Pearl Islands (Gulf of Panama) in relation to thermal conditions. Limnol Oceanogr 18:367–379

    Article  Google Scholar 

  45. Gori A, Orejas C, Madurell T, Bramanti L, Martins M, Quintanilla E, Marti-Puig P, Lo Iacono C, Puig P, Requena S, Greenacre M, Gili JM (2013) Bathymetrical distribution and size structure of cold-water coral populations in the Cap de Creus and Lacaze-Duthiers canyons (northwestern Mediterranean). Biogeosciences 10:2049–2060

    Article  Google Scholar 

  46. Henry LA, Roberts JM (2007) Biodiversity and ecological composition of macrobenthos on cold-water coral mounds and adjacent off-mound habitat in the bathyal Porcupine Seabight, NE Atlantic. Deep Sea Res Part 1 Oceanogr Res Pap 54:654–672

  47. Holmes RM, Aminot A, Kérouel R, Hooker BA, Peterson BJ (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56:1801–1808

    CAS  Article  Google Scholar 

  48. Howe SA, Marshall AT (2001) Thermal compensation of metabolism in the temperate coral Plesiastrea versipora (Lamark 1816). J Exp Mar Biol Ecol 259:231–248

    PubMed  Article  Google Scholar 

  49. Howe SA, Marshall AT (2002) Temperature effects on calcification rate and skeletal deposition in the temperate coral Plesiastrea versipora (Lamarck). J Exp Mar Biol Ecol 275:63–81

    CAS  Article  Google Scholar 

  50. Huvenne VAI, Tyler PA, Masson DG, Fisher EH, Hauton C, Hühnerbach V, Le Bas TP, Wolff GA (2011) A picture on the wall: innovative mapping reveals cold-water coral refuge in submarine canyon. PLoS One 6:e28755

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  51. Ip YK, Lim LL, Lim RWL (1991) Some properties of calcium-activated adenosine triphosphate from the hermatypic coral Galaxea fascicularis. Mar Biol 111:191–197

    CAS  Article  Google Scholar 

  52. 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

    CAS  Article  Google Scholar 

  53. Jacques TG, Marshall N, Pilson MEQ (1983) Experimental ecology of the temperate scleractinian coral Astrangia danae. II Effect of temperature, light intensity and symbiosis with zooxanthellae on metabolic rate and calcification. Mar Biol 76:135–148

    CAS  Article  Google Scholar 

  54. Jokiel PL, Coles SL (1977) Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar Biol 43:201–208

    Article  Google Scholar 

  55. Jokiel PL, Maragos JE, Franzisket L (1978) Coral growth: buoyant weight technique. In: Stoddard JR, Johannes RE (eds) Coral reefs: research methods. UNESCO, Paris

    Google Scholar 

  56. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386

    Article  Google Scholar 

  57. Kang CK (1999) Structures trophiques et production secondaire dans les réseaux benthiques intertidaux du bassin de Marennes-Oléron: utilisation du traçage isotopique naturel. Ph.D. thesis, University of Nantes, Nantes, France

  58. Kemp DW, Oakley CA, Thornhill DJ, Newcomb LA, Schmidt GW, Fitt WK (2011) Catastrophic mortality on inshore coral reefs of the Florida Keys due to severe low-temperature stress. Glob Change Biol 17:3468–3477

    Article  Google Scholar 

  59. Kevin KM, Hudson RCL (1979) The role of zooxanthellae in the hermatypic coral Plesiastrea urvillei (Milne Edwards and Haime) from cold waters. J Exp Mar Biol Ecol 36:157–170

    Article  Google Scholar 

  60. Krieger KJ, Wing B (2002) Megafauna associations with deepwater corals (Primnoa sp.) in the Gulf of Alaska. Hydrobiologia 471:83–90

    Article  Google Scholar 

  61. Langdon C, Gattuso JP, Andersson A (2010) Measurement of calcification and dissolution of benthic organisms and communities. In: Riebesell U, Fabry VJ, Hanson L, Gattuso JP (eds) Guide to best practices for ocean acidification research and data reporting. Publications office of the European Union, Luxembourg

    Google Scholar 

  62. Le Danois E (1948) Les profondeurs de la mer. Payot, Paris

    Google Scholar 

  63. Lewis JB, Price WS (1975) Feeding mechanisms and feeding strategies of Atlantic reef corals. J Zool Lond 176:527–544

    Article  Google Scholar 

  64. Lough JM, Barnes DJ (2000) Environmental controls on growth of the massive coral Porites. J Exp Mar Biol Ecol 245:225–243

    PubMed  Article  Google Scholar 

  65. Maier C, Hegeman J, Weinbauer MG, Gattuso JP (2009) Calcification of the cold-water coral Lophelia pertusa under ambient and reduced pH. Biogeosciences 6:1875–1901

    Article  Google Scholar 

  66. Maier C, Watremez P, Taviani M, Weinbauer MG, Gattuso JP (2012) Calcification rates and the effect of ocean acidification on Mediterranean cold-water corals. Proc R Soc Lond B Biol Sci 279:1716–1723

    CAS  Article  Google Scholar 

  67. Marshall AT, Clode P (2004) Calcification rate and the effect of temperature in a zooxanthellate and an azooxanthellate scleractinian reef coral. Coral Reefs 23:218–224

    Google Scholar 

  68. Miller RJ, Hocevar J, Stone RP, Fedorov DV (2012) Structure-forming corals and sponges and their use as fish habitat in Bering Sea submarine canyons. PLoS One 7:e33885

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  69. Movilla J, Orejas C, Calvo E, Gori A, López-Sanz À, Grinyó J, Domínguez-Carrió C, Pelejero C (2014) Differential response of two Mediterranean cold-water coral species to ocean acidification. Coral Reefs. doi:10.1007/s00338-014-1159-9

    Google Scholar 

  70. Naumann MS, Orejas C, Ferrier-Pagès C (2013) High thermal tolerance of two Mediterranean cold-water coral species maintained in aquaria. Coral Reefs 32:749–754

    Article  Google Scholar 

  71. Naumann MS, Orejas C, Ferrier-Pagès C (2014) Species-specific physiological response by the cold-water corals Lophelia pertusa and Madrepora oculata to variations within their natural temperature range. Deep Sea Res Part 2 Top Stud Oceanogr 99:36–41

  72. Naumann MS, Orejas C, Wild C, Ferrier-Pagès C (2011) First evidence for zooplankton feeding sustaining key physiological processes in a scleractinian cold-water coral. J Exp Biol 214:3570–3576

    CAS  PubMed  Article  Google Scholar 

  73. Naumann MS, Niggl W, Laforsch C, Glaser C, Wild C (2009) Coral surface area quantification - evaluation of established methods by comparison with computer tomography. Coral Reefs 28:109–117

    Article  Google Scholar 

  74. Naumann MS, Haas A, Struck U, Mayr C, el-Zibdah M, Wild C (2010) Organic matter release by dominant hermatypic corals of the Northern Red Sea. Coral Reefs 29:649–659

    Article  Google Scholar 

  75. Olariaga A, Gori A, Orejas C, Gili JM (2009) Development of an autonomous aquarium system for maintaining deep corals. Oceanography 22:44–45

    Article  Google Scholar 

  76. Orejas C, Gori A, Lo Iacono C, Puig P, Gili JM (2009) Cold-water corals in the Cap de Creus canyon, northwestern Mediterranean: spatial distribution, density and anthropogenic impact. Mar Ecol Prog Ser 397:37–51

    Article  Google Scholar 

  77. Orejas C, Ferrier-Pagès C, Reynaud S, Gori A, Beraud E, Tsounis G, Allemand D, Gili JM (2011a) Long-term growth rate measurements of four Mediterranean cold water coral species (Madrepora oculata, Lophelia pertusa, Desmophyllum cristagalli and Dendrophyllia cornigera) maintained in aquaria. Mar Ecol Prog Ser 429:57–65

    Article  Google Scholar 

  78. Orejas C, Ferrier-Pagès C, Reynaud S, Tsounis G, Allemand D, Gili JM (2011b) Experimental comparison of skeletal growth rates in the cold-water coral Madrepora oculata Linnaeus, 1758 and three tropical scleractinian corals. J Exp Mar Biol Ecol 405:1–5

    Article  Google Scholar 

  79. Pérès JM, Picard J (1964) Nouveau manuel de bionomie benthique de la mer Mediterranée. Station Marine d’Endoume 31:5–137

    Google Scholar 

  80. Previati M, Scinto A, Cerrano C, Osinga R (2010) Oxygen consumption in Mediterranean octocorals under different temperatures. J Exp Mar Biol Ecol 390:39–48

    Article  Google Scholar 

  81. Purser A, Orejas C, Gori A, Tong T, Unnithan V, Thomsen L (2013) Local variation in the distribution of benthic megafauna species associated with cold-water coral reefs on the Norwegian margin. Cont Shelf Res 54:37–51

    Article  Google Scholar 

  82. R Core Development Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051- 07-0, URL. http://www.R-project.org

  83. Reed JK (1981) In situ growth rates of the scleractinian coral Oculina varicosa occurring with zooxanthellae on 6 m reefs and without on 80 m banks. Proc 4th Int Coral Reef Symp 2:201–206

  84. Reveillaud J, Freiwald A, Van Rooij D, Le Guilloux E, Altuna A, Foubert A, Vanreusel A, Olu-Le Roy K, Henriet JP (2008) The distribution of scleractinian corals in the Bay of Biscay, NE Atlantic. Facies 54:317–331

    Article  Google Scholar 

  85. Ribes M, Coma R, Rossi S (2003) Natural feeding of the temperate asymbiotic octocoral-gorgonian Leptogorgia sarmentosa (Cnidaria: Octocorallia). Mar Ecol Prog Ser 254:141–150

    CAS  Article  Google Scholar 

  86. Roberts JM, Wheeler AJ, Freiwald A (2006) Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312:543–547

    CAS  PubMed  Article  Google Scholar 

  87. Roberts JM, Wheeler AJ, Freiwald A, Cairns S (2009a) Cold-water corals: the biology and geology of deep-sea coral habitats. Cambridge University Press, Cambridge

    Google Scholar 

  88. Roberts JM, Davies AJ, Henry LA, Dodds LA, Duineveld GCA, Lavaleye MSS, Maier C, van Soest RWM, Bergman MJN, Hühnerbach V, Huvenne VAI, Sinclair DJ, Watmough T, Long D, Green SL, van Haren H (2009b) Mingulay reef complex: an interdisciplinary study of cold-water coral habitat, hydrography and biodiversity. Mar Ecol Prog Ser 397:139–151

    CAS  Article  Google Scholar 

  89. Rodolfo-Metalpa R, Richard C, Allemand D, Ferrier-Pagès C (2006) Growth and photosynthesis of two Mediterranean corals, Cladocora caespitosa and Oculina patagonica, under normal and elevated temperatures. J Exp Biol 209:4546–4556

    PubMed  Article  Google Scholar 

  90. Rodolfo-Metalpa R, Reynaud S, Allemand D, Ferrier-Pagès C (2008a) Temporal and depth response of two temperate corals, Cladocora caespitosa and Oculina patagonica from the north Mediterranean Sea. Mar Ecol Prog Ser 369:103–114

    Article  Google Scholar 

  91. Rodolfo-Metalpa R, Peirano A, Houlbrèque F, Abbate M, Ferrier-Pagès C (2008b) Effects of temperature, light and heterotrophy on the growth of the temperate coral Cladocora caespitosa. Coral Reefs 27:17–25

    Article  Google Scholar 

  92. Salomidi M, Zibrowius H, Issaris Y, Milionis K (2010) Dendrophyllia in Greek waters, Mediterranean Sea, with first record of D. ramea (Cnidaria, Scleractinia) from the area. Mediterr Mar Sci 11:189–194

    Article  Google Scholar 

  93. Sánchez F, Serrano A, Ballesteros MG (2009) Photogrammetric quantitative study of habitat and benthic communities of deep Cantabrian Sea hard grounds. Cont Shelf Res 29:1174–1188

    Article  Google Scholar 

  94. Sassaman C, Mangum CP (1970) Patterns of temperature adaptation in North American Atlantic coastal actinians. Mar Biol 7:123–130

    Article  Google Scholar 

  95. Schutter M, Crocker J, Paijmans A, Janse M, Osinga R, Verreth AJ, Wijffels RH (2010) The effect of different flow regimes on the growth and metabolic rates of the scleractinian coral Galaxea fascicularis. Coral Reefs 29:737–748

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  97. Valencia V, Franco J, Borja Á, Fontán A (2004) Hydrography of the southeastern Bay of Biscay. Elsevier Oceanography Series 70:159–194

    Article  Google Scholar 

  98. Van Oevelen D, Duineveld G, Lavaleye M, Mienis F, Soetaert K, Heip CHR (2009) The cold-water coral community as a hot spot for carbon cycling on continental margins: A food-web analysis from Rockall Bank (northeast Atlantic). Limnol Oceanogr 54:1829–1844

    Article  Google Scholar 

  99. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee JC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395

    CAS  PubMed  Article  Google Scholar 

  100. Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYW, Jørgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70

    CAS  PubMed  Article  Google Scholar 

  101. Wild C, Wehrmann LM, Mayr C, Schöttner SI, Allers E, Lundälv T (2009) Microbial degradation of cold-water coral-derived organic matter: potential implication for organic C cycling in the water column above Tisler Reef. Aquat Biol 7:71–80

    Article  Google Scholar 

  102. Wild C, Mayr C, Wehrmann L, Schöttner S, Naumann M, Hoffmann F, Rapp HT (2008) Organic matter release by cold water corals and its implication for fauna–microbe interaction. Mar Ecol Prog Ser 372:67–75

    CAS  Article  Google Scholar 

  103. Wildish D, Kristmanson D (1997) Benthic suspension feeders and flow. Cambridge University Press, Cambridge

    Google Scholar 

  104. Zibrowius H (1980) Les scléractiniaires de la Méditerranée et de l’Atlantique nord-oriental. Memoires de I’Institut océanographique, Monaco 11:1–284

    Google Scholar 

Download references

Acknowledgments

The authors are indebted to the crew and scientists on board the RV ‘García del Cid’, as well as to the JAGO team, J. Schauer and K. Hissmann (IFM-GEOMAR, Kiel, Germany) for their help during the coral collection. We are grateful to A. Olariaga, C. Domínguez-Carrió, J. Grinyó, and S. Ambroso for helping with the coral care in Barcelona, to the personnel from the Musée Océanographique de Monaco for helping with the coral care in Monaco, to P.J. López-González for the picture in Fig. 1, A. Braga-Henriques, A. Brito and M. Bo for information about D. cornigera occurrence and seawater temperature, to S. Sikorski and C. Rottier for laboratory assistance, to A. Venn and S. Hennige for revision of the English, and to D. Allemand for discussions. This work was supported by the Government of the Principality of Monaco, and by the European Project LIFE + INDEMARES ‘Inventario y designación de la red natura 2000 en áreas marinas del estado español’ (LIFE07/NAT/E/000732), and HERMIONE (Grant Agreement Number 226354).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Andrea Gori.

Additional information

Communicated by Biology Editor Dr. Anastazia Banaszak

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 50 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gori, A., Reynaud, S., Orejas, C. et al. Physiological performance of the cold-water coral Dendrophyllia cornigera reveals its preference for temperate environments. Coral Reefs 33, 665–674 (2014). https://doi.org/10.1007/s00338-014-1167-9

Download citation

Keywords

  • Physiological ecology
  • Thermal tolerance
  • Coral calcification
  • Coral growth
  • Coral respiration
  • Organic carbon fluxes