Coral Reefs

, Volume 35, Issue 3, pp 1033–1045 | Cite as

Variation in lipid and free fatty acid content during spawning in two temperate octocorals with different reproductive strategies: surface versus internal brooder

  • Núria Viladrich
  • Lorenzo Bramanti
  • Georgios Tsounis
  • Blanca Chocarro
  • Angela Martínez-Quitana
  • Stefano Ambroso
  • Teresa Madurell
  • Sergio Rossi
Report

Abstract

This study investigates the energetic investment during spawning of two Mediterranean gorgonians characterized by different reproductive strategies: Corallium rubrum (internal brooder) and Paramuricea clavata (surface brooder). Sexual products (number of oocytes and spermatic sacs) were quantified, and biochemical characteristics (lipid content and free fatty acid content and composition) were determined to investigate the parental energetic investment and demand in reproduction. Results suggested that the majority of the energetic cost was due to reproductive activity (i.e., gametogenesis and spawning). The two species exhibited different life history strategies, with P. clavata investing more energy in reproduction than C. rubrum. However, P. clavata is reproductively more sensitive to inter-annual changes in environmental conditions.

Keywords

Energy investment Free fatty acids Lipids Corallium rubrum Paramuricea clavata 

Supplementary material

338_2016_1440_MOESM1_ESM.docx (102 kb)
Supplementary material 1 (DOCX 102 kb)

References

  1. Al-lihlaibi SS, Al-Sofyani AA, Niaz GR (1998) Chemical composition of corals in Saudi Red Sea Coast. Oceanologica Acta 21:495–501CrossRefGoogle Scholar
  2. Allemand D, Tambutté E, Zoccola D, Tambutté S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Netherlands, pp 119–150CrossRefGoogle Scholar
  3. Arai T, Kato M, Heyward A, Ikeda Y, Iizuka Y, Murayama T (1993) Lipid composition of positively buoyant eggs of reef-building corals. Coral Reefs 12:71–75CrossRefGoogle Scholar
  4. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195CrossRefGoogle Scholar
  5. Baptista M, Lopes VM, Pimentel MS, Bandarra N, Narciso L, Marques A, Rosa R (2012) Temporal fatty acid dynamics of the octocoral Veretillum cynomorium. Comp Biochem Physiol B 161:178–187CrossRefPubMedGoogle Scholar
  6. Barnes H, Blackstock J (1973) Estimation of lipids in marine animals’ tissues: detailed investigation of the sulphophosphovanillin method for “total” lipids. J Exp Mar Bio Ecol 12:103–118CrossRefGoogle Scholar
  7. Bayne BL, Gabbott PA, Widdows J (1975) Some effects of stress in the adults on the eggs and larvae of Mytilus edulis. J Mar Biol Assoc UK 55:675–689CrossRefGoogle Scholar
  8. Bramanti L, Magagnini G, De Maio L, Santangelo G (2005) Recruitment, early survival and growth of the Mediterranean red coral Corallium rubrum (L. 1758), a 4-year study. J Exp Mar Bio Ecol 314:69–78CrossRefGoogle Scholar
  9. Brey T (1995) Temperature and reproductive metabolism in macrobenthic populations. Mar Ecol Prog Ser 125:87–93CrossRefGoogle Scholar
  10. Cantin NE, Negri AP, Willis BL (2007) Photoinhibition from chronic herbicide exposure reduces reproductive output of reef-building corals. Mar Ecol Prog Ser 344:81–93CrossRefGoogle Scholar
  11. Cerrano C, Bavestrello G, Bianchi CN, Cattaneo-Vietti R, Bava S, Morganti C, Morri C, Picco P, Sara G, Schiaparelli S, Siccardi A, Sponga F (2000) A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (NW Mediterranean), summer 1999. Ecol Lett 3:284–293CrossRefGoogle Scholar
  12. Chambers JM, Hastie TJ (1992) Statistical models in S. CRC Press, Boca Raton, FL, USAGoogle Scholar
  13. Coma R, Ribes M (2003) Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization. Oikos 101:205–215CrossRefGoogle Scholar
  14. Coma R, Gili JM, Zabala M, Riera T (1994) Feeding and prey capture cycles in the aposymbiontic gorgonian Paramuricea clavata. Mar Ecol Prog Ser 115:257–270CrossRefGoogle Scholar
  15. Coma R, Ribes M, Zabala M, Gili JM (1995) Reproduction and cycle of gonadal development in the Mediterranean gorgonian Paramuricea clavata. Mar Ecol Prog Ser 117:173–183CrossRefGoogle Scholar
  16. Coma R, Ribes M, Gili JM, Zabala M (1998) An energetic approach to the study of life history of two modular colonial invertebrates. Mar Ecol Prog Ser 162:89–103CrossRefGoogle Scholar
  17. Coma R, Ribes M, Gili JM, Zabala M (2000) Seasonality in coastal benthic ecosystems. Trends Ecol Evol 15:448–453CrossRefPubMedGoogle Scholar
  18. Cupido R, Cocito S, Manno V, Ferrando S, Peirano A, Iannelli M, Bramanti L, Santangelo G (2012) Sexual structure of a highly reproductive, recovering gorgonian population: quantifying reproductive output. Mar Ecol Prog Ser 469:25–36CrossRefGoogle Scholar
  19. Dalsgaard J, St John M, Kattner G, Muller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340CrossRefPubMedGoogle Scholar
  20. Debreuil J, Tambutté S, Zoccola D, Segonds N, Techer N, Allemand D, Tambutté É (2011) Comparative analysis of the soluble organic matrix of axial skeleton and sclerites of Corallium rubrum: insights for biomineralization. Comp Biochem Physiol B 159:40–48CrossRefPubMedGoogle Scholar
  21. Díaz-Almeyda E, Thomé P, El Hafidi M, Iglesias-Prieto R (2011) Differential stability of photosynthetic membranes and fatty acid composition at elevated temperature in Symbiodinium. Coral Reefs 30:217–225CrossRefGoogle Scholar
  22. Doughty P, Shine R (1997) Detecting life history trade-offs: measuring energy stores in “capital” breeders reveals costs of reproduction. Oecologia 110:508–513CrossRefGoogle Scholar
  23. Ennever J, Vogel JJ, Streckfues (1971) Synthetic medium for calcification of Bacterionema matruchottii. J Dent Res 50:1327–1330CrossRefPubMedGoogle Scholar
  24. Fiorillo I, Rossi S, Alva V, Gili JM, López-González PJ (2013) Seasonal cycle of sexual reproduction of the Mediterranean soft coral Alcyonium acaule (Anthozoa, Octocorallia). Mar Biol 160:719–728CrossRefGoogle Scholar
  25. Garrabou J, Harmelin JG (2002) A 20-year study on life-history traits of a harvested long-lived temperate coral in the NW Mediterranean: insights into conservation and management needs. J Anim Ecol 71:966–978CrossRefGoogle Scholar
  26. Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonné P, Ciglianos M, Díaz D, Harmelin JG, Gambis MC, Kersting DK, Ledoux JB, Lejeusne C, Linares C, Marschal C, Pérez T, Ribes M, Romano JC, Serrano E, Teixidó N, Torrents O, Zabala M, Zuberer F, Cerrano C (2009) Mass mortality in northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Chang Biol 15:1090–1103CrossRefGoogle Scholar
  27. Giese AC (1959) Reproductive cycles of some west coast invertebrates. Symposium on photoperiodism in plants and animals, Gatlinburg, 1957. A.A.A.S., Washington, D.CGoogle Scholar
  28. Giesel JT (1976) Reproductive strategies as adaptations to life in temporally heterogeneous environments. Annu Rev Ecol Syst 7:57–79CrossRefGoogle Scholar
  29. Gili JM, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Tree 13:316–321PubMedGoogle Scholar
  30. Gori A, Viladrich N, Gili JM, Kotta M, Cucio C, Magni L, Rossi S (2012) Reproductive cycle and trophic ecology in deep versus shallow populations of the Mediterranean gorgonian Eunicella singularis (Cap de Creus, northwestern Mediterranean Sea). Coral Reefs 31:823–837CrossRefGoogle Scholar
  31. Gori A, Linares C, Viladrich N, Clavero A, Orejas C, Fiorillo I, Ambroso S, Gili JM, Rossi S (2013) Effects of food availability on the sexual reproduction and biochemical composition of the Mediterranean gorgonian Paramuricea clavata. J Exp Mar Bio Ecol 444:38–45CrossRefGoogle Scholar
  32. Grémare A, Amouroux JM, Charles F, Dinet A, Riaux-Gobin C, Baudart J, Medernach L, Bodiou JY, Vétion G, Colomines JC, Albert P (1997) Temporal changes in the biochemical composition and nutritional value of the particulate organic matter available to surface deposit-feeders: a two year study. Mar Ecol Prog Ser 150:195–206CrossRefGoogle Scholar
  33. Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol 145:621–631CrossRefGoogle Scholar
  34. Gurr MI, Harwood JL, Frayn KN (2002) Lipid biochemistry. Blackwell Science, Oxford, UKCrossRefGoogle Scholar
  35. Gutierrez-Rodrigues C, Lasker HR (2004) Microsatellite variation reveals high levels of genetic variability and population structure in the gorgonian coral Pseudopterogorgia elisabethae across the Bahamas. Mol Ecol 13:2211–2221CrossRefGoogle Scholar
  36. Hall JM, Parrish CC, Thompson RJ (2000) Importance of unsaturated fatty acids in regulating bivalve and finfish membrane fluidity in response to changes in environmental temperature. In: Shahidi F (ed) Seafood in health and nutrition. ScienceTech Publishing, St. John’s, Canada, pp 435–448Google Scholar
  37. Harii S, Kayanne H, Takigawa H, Hayashibara T, Yamamoto M (2002) Larval survivorship, competency periods and settlement of two brooding corals, Heliopora coerulea and Pocillopora damicornis. Mar Biol 141:39–46CrossRefGoogle Scholar
  38. Harms J (1992) Larval development and delayed metamorphosis in the hermit crab Clibanarius erythropus (Latreille) (Crustacea, Diogenidae). J Exp Mar Bio Ecol 156:151–160CrossRefGoogle Scholar
  39. Imbs AB (2013) Fatty acids and other lipids of corals: composition, distribution, and biosynthesis. Russ J Mar Biol 39:153–168CrossRefGoogle Scholar
  40. Imbs AB, Dautova TN (2008) Use of lipids for chemotaxonomy of octocorals (Cnidaria: Alcyonaria). Russ J Mar Biol 34:174–178CrossRefGoogle Scholar
  41. Imbs AB, Latyshev NA, Dautova TN, Latypov YY (2010) Distribution of lipids and fatty acids in corals by their taxonomic position and presence of zooxanthellae. Mar Ecol Prog Ser 409:55–65CrossRefGoogle Scholar
  42. Imbs AB, Dang LP, Rybin VG, Svetashev VI (2015) Fatty acid, lipid class, and phospholipid molecular species composition of the soft coral Xenia sp. (Nha Trang Bay, the South China Sea, Vietnam). Lipids 50:575–589CrossRefPubMedGoogle Scholar
  43. Jablonski D, Lutz RA (1983) Larval ecology of marine benthic invertebrates —paleobiological implications. Biol Rev Camb Philos Soc 58:21–89CrossRefGoogle Scholar
  44. Kahng SE, Benayahu Y, Lasker HR (2011) Sexual reproduction in octocorals. Mar Ecol Prog Ser 443:265–283CrossRefGoogle Scholar
  45. Lawrence JM, McClintock JB (1994) Energy acquisition and allocation by echinoderms (Echinodermata) in polar seas: adaptations for success? In: David B, Guille A, Féral JP, Roux M (eds) Echinodermata. Balkema, Rotterdam, pp 39–52Google Scholar
  46. Lehninger AL (1982) Principles of biochemistry. Worth, New YorkGoogle Scholar
  47. Lenz EA, Bramanti L, Lasker HR, Edmunds PJ (2015) Long-term variation of octocoral populations in St. John, US Virgin Islands. Coral Reefs 34:1099–1109CrossRefGoogle Scholar
  48. Leuzinger S, Anthony KRN, Willis BL (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136:524–531CrossRefPubMedGoogle Scholar
  49. MacGinitie GE, MacGinitie N (1949) Natural history of marine animals. McGraw-Hill, New YorkGoogle Scholar
  50. Meijer L, Guerrier P, McClouf J (1984) Arachidonic acid, 12- and 15-hydroxyeicosatetraenoic acids, eicosapentaenoic acid, and phospholipase A2 induce starfish oocyte maturation. Dev Biol 106:368–378CrossRefPubMedGoogle Scholar
  51. Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, OxfordGoogle Scholar
  52. Müller-Navarra DC, Brett MT, Liston AM, Goldman CR (2000) A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers. Nature 403:74–77CrossRefPubMedGoogle Scholar
  53. Oksanen J, Kindt R, Legendre P, O’Hara RB (2005) Vegan: community ecology package. Version 1.7–81. http://cran.r-project.org
  54. Orejas C, Lopez-Gonzalez PJ, Gili JM, Teixidó N, Gutt J, Arntz WE (2002) Distribution and reproductive ecology of the Antarctic octocoral Ainigmaptilon antarcticum in the Weddell Sea. Mar Ecol Prog Ser 231:101–114CrossRefGoogle Scholar
  55. Pechenik JA (1990) Delayed metamorphosis by larvae of benthic marine invertebrates: does it occur? Is there a price to pay? Ophelia 32:63–94CrossRefGoogle Scholar
  56. Pérez MJ, Rodríguez C, Cejas JR, Martín MV, Jerez S, Lorenzo A (2007) Lipid and fatty acid content in wild white seabream (Diplodus sargus) broodstock at different stages of the reproductive cycle. Comp Biochem Physiol B Biochem Mol Biol 146:187–196CrossRefPubMedGoogle Scholar
  57. Pernet V, Gavino V, Gavino G, Anctil M (2002) Variations of lipid and fatty acid contents during the reproductive cycle of the anthozoan Renilla koellikeri. J Comp Physiol B 172:455–465CrossRefPubMedGoogle Scholar
  58. Previati M, Scinto A, Cerrano C, Osinga R (2010) Oxygen consumption in Mediterranean octocorals under different temperatures. J Exp Mar Bio Ecol 390:39–48CrossRefGoogle Scholar
  59. Qian PY, Chia FS (1991) Fecundity and egg size were mediated by quality of diet in the marine polychaete worm, Capitella sp. J Exp Mar Bio Ecol 148:11–25CrossRefGoogle Scholar
  60. Qian PY, Chia FS (1992) Effects of diet type on the demographics of Capitella sp. (Annelida: Polychaeta): lecithotrophic development vs. planktotrophic development. J Exp Mar Bio Ecol 157:159–179CrossRefGoogle Scholar
  61. R Development Core Team (2008) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  62. Raymond JF, Himmelman JH, Guderley HE (2007) Biochemical content, energy composition and reproductive effort in the broadcasting sea star Asterias vulgaris over the spawning period. J Exp Mar Bio Ecol 341:32–44CrossRefGoogle Scholar
  63. Ribes M, Coma R, Gili JM (1999) Heterogeneous feeding in benthic suspension feeders: the natural diet and grazing rate of the temperate gorgonian Paramuricea clavata (Cnidaria: Octocorallia) over a year cycle. Mar Ecol Prog Ser 183:125–137CrossRefGoogle Scholar
  64. Ribes M, Coma R, Rossi S, Michelli M (2007) The cycle of gonadal development of Eunicella singularis (Cnidaria: Octocorallia). Invertebr Biol 126:307–317CrossRefGoogle Scholar
  65. Roff DA (2002) Life history evolution. Sinauer Associates, Sunderland, MAGoogle Scholar
  66. Rossi S (2013) The destruction of the “animal forests” in the oceans: towards an over-simplification of the benthic ecosystems. Ocean Coast Manag 84:77–85CrossRefGoogle Scholar
  67. Rossi S, Tsounis G (2007) Temporal and spatial variation in protein, carbohydrate, and lipid levels in Corallium rubrum (Anthozoa, Octocorallia). Mar Biol 152:429–439CrossRefGoogle Scholar
  68. Rossi S, Gili JM (2009) The cycle of gonadal development of the soft bottom-gravel gorgonian Leptogorgia sarmentosa (Esper, 1791) in the NW Mediterranean sea. Invertebr Reprod Dev 53:175–190CrossRefGoogle Scholar
  69. Rossi S, Fiorillo I (2010) Biochemical features of a Protoceratium reticulatum red tide in Chipana Bay (northern Chile) in summer conditions. Sci Mar 74:633–642CrossRefGoogle Scholar
  70. Rossi S, Ribes M, Coma R, Gili JM (2004) Temporal variability in zooplankton prey capture of the passive suspension feeder Leptogorgia sarmentosa (Cnidaria: Octocorallia) a case study. Mar Biol 144:89–99CrossRefGoogle Scholar
  71. Rossi S, Grémare A, Gili JM, Amouroux JM, Jordana E, Vétion G (2003) Biochemical characteristics of settling particulate organic matter at two north–western Mediterranean sites: a seasonal comparison. Estuar Coast Shelf S58:423–434CrossRefGoogle Scholar
  72. Rossi S, Gili JM, Coma R, Linares C, Gori A, Vert N (2006) Temporal variation in protein, carbohydrate, and lipid concentrations in Paramuricea clavata (Anthozoa, Octocorallia): evidence for summer–autumn feeding constraints. Mar Biol 149:643–651CrossRefGoogle Scholar
  73. Santangelo G, Maggi E, Bramanti L, Bongiorni L (2003) Demography of the over-exploited Mediterranean red coral (Corallium rubrum L. 1758). Sci Mar 68:199–204CrossRefGoogle Scholar
  74. Santangelo G, Cupido R, Cocito S, Bramanti L, Priori C, Erra F, Iannelli M (2015) Effects of increased mortality on gorgonian corals (Cnidaria, Octocorallia): different demographic features may lead affected populations to unexpected recovery and new equilibrium points. Hydrobiologia 759:171–187CrossRefGoogle Scholar
  75. Sargent JR, Parks RJ, Mueller-Harvey I, Henderson RJ (1988) Lipid biomarkers in marine ecology. In: Sliegh MA (ed) Microbes in the sea. Ellis Horwood Ltd, Chichester, pp 119–138Google Scholar
  76. Sargent JR, McEvoy LA, Estevez A, Bell JG, Bell M, Henderson J, Tocher D (1999) Lipid nutrition of marine fish during early development: current status and future directions. Aquaculture 179:217–229CrossRefGoogle Scholar
  77. Schols P, Lorson D (2008) Macnification. Orbicule, Leuven, Belgium, www.orbicule.com
  78. Sebens KP (1987) Coelenterata. In: Pandian TJ, Vernberg FJ (eds) Animals energetics. Academic, San Diego, pp 55–120Google Scholar
  79. Sebens KP, Vandersall KS, Savina LA, Graham KR (1996) Zooplankton capture by two scleractinian corals, Madracis mirabilis and Montastrea cavernosa, in a field enclosure. Mar Biol 127:303–317CrossRefGoogle Scholar
  80. Slattery M, McClintock JB (1995) Population structure and feeding deterrence in three shallow-water Antarctic soft corals. Mar Biol 122:461–470CrossRefGoogle Scholar
  81. Stanley-Samuelson DW (1987) Physiological roles of prostaglandins and other eicosanoids in invertebrates. Biol Bull 173:92–109CrossRefGoogle Scholar
  82. Stearns SC (1992) The evolution of life histories. Oxford University Press, New YorkGoogle Scholar
  83. Stimson JS (1987) Location, quantity and rate of change in quantity of lipids in tissue of Hawaiian hermatypic corals. Bull Mar Sci 41:889–904Google Scholar
  84. Strathmann RR (1977) Egg size, larval development, and juvenile size in benthic marine invertebrates. Am Nat 111:373–376CrossRefGoogle Scholar
  85. Tsounis G, Rossi S, Gili JM, Arntz WE (2007) Red coral fishery at the Costa Brava (NW Mediterranean): case study of an overharvested precious coral. Ecosystems 10:975–986CrossRefGoogle Scholar
  86. Tsounis G, Rossi S, Aranguren M, Gili JM, Arntz WE (2006a) Effects of spatial variability and colony size on the reproductive output and gonadal development cycle of the Mediterranean red coral (Corallium rubrum L.). Mar Biol 148:513–527CrossRefGoogle Scholar
  87. Tsounis G, Rossi S, Laudien J, Bramanti L, Fernández N, Gili JM, Arntz W (2006b) Diet and seasonal prey capture rate in the Mediterranean red coral (Corallium rubrum L.). Mar Biol 149:313–325CrossRefGoogle Scholar
  88. Tsounis G, Martínez L, Viladrich N, Bramanti L, Martínez A, Gili JM, Rossi S (2012) Effects of human impact on the reproductive effort and allocation of energy reserves in the Mediterranean octocoral Paramuricea clavata. Mar Ecol Prog Ser 449:161–172CrossRefGoogle Scholar
  89. Turon X, Becerro MA (1992) Growth and survival of several ascidian species from the northwestern Mediterranean. Mar Ecol Prog Ser 82:235–247CrossRefGoogle Scholar
  90. Varvas K, Jarving I, Koljak R, Vahemets A, Pehk T, Müürisepp AM, Lille U, Samel N (1993) Invitro biosynthesis of prostaglandins in the White Sea soft coral Gersemia-Fruticosa — formation of optically-active Pgd2, Pge2, Pgf2-alpha and 15-keto-Pgf2-alpha from arachidonic-acid. Tetrahedron Lett 34:3643–3646CrossRefGoogle Scholar
  91. Vighi M (1972) Ètude sur la reproduction du Corallium rubrum (L.). Vie Milieu Paris 23:21–32Google Scholar
  92. Viladrich N, Rossi S, López-Sanz A, Orejas C (2015) Nutritional condition of two coastal rocky fishes and the potential role of a marine protected area. Mar Ecol 37:46–63CrossRefGoogle Scholar
  93. Wacker A, von Elert E (2001) Polyunsaturated fatty acids: evidence for non-substitutable biochemical resources in Daphnia galeata. Ecology 82:2507–2520CrossRefGoogle Scholar
  94. Ward S (1995) The effect of damage on the growth, reproduction and storage of lipids in the scleractinian coral Pocillopora damicornis (Linnaeus). J Exp Mar Bio Ecol 187:193–206CrossRefGoogle Scholar
  95. Weinheimer AJ, Spraggins RL (1969) The occurrence of two new prostaglandin derivatives (l5-epi-PGA2 and its acetate methyl ester) in the gorgonian Plexaura homomalla: chemistry of coelenterates XV. Tetrahedron Lett 59:5185–5188CrossRefPubMedGoogle Scholar
  96. Wild C, Hoegh-Guldberg O, Naumann MS, Colombo-Pallotta MF, Ateweberhan M, Fitt WK, Iglesias-Prieto R, Palmer C, Bythell JC, Ortiz JC, Loya Y, van Woesik R (2011) Climate change impedes scleractinian corals as primary reef ecosystem engineers. Mar Freshw Res 62:205–215CrossRefGoogle Scholar
  97. Yamashiro H, Oku H, Onaga K (2005) Effect of bleaching on lipid content and composition of Okinawan corals. Fish Sci 71:448–453CrossRefGoogle Scholar
  98. Yamashiro H, Oku H, Onaga K, Iwasaki H, Takara K (2001) Coral tumors store reduced level of lipids. J Exp Mar Bio Ecol 265:171–179CrossRefGoogle Scholar
  99. Young SD, O’Connor JD, Muscatine L (1971) Organic material from scleractinian coral skeletons. II. Incorporation of 14C into protein, chitin and lipid. Comp Biochem Physiol B 40:945–958CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Núria Viladrich
    • 1
  • Lorenzo Bramanti
    • 2
    • 3
  • Georgios Tsounis
    • 4
  • Blanca Chocarro
    • 1
  • Angela Martínez-Quitana
    • 4
  • Stefano Ambroso
    • 4
  • Teresa Madurell
    • 4
  • Sergio Rossi
    • 1
  1. 1.Institut de Ciència i Tecnologia AmbientalsUniversitat Autònoma de BarcelonaCerdanyola Del VallèsSpain
  2. 2.UPMC Univ Paris 06, CNRS, Laboratoire d’Ecogéochimie des Environnements Benthiques (LECOB), Observatoire OcéanologiqueSorbonne UniversitésBanyuls/MerFrance
  3. 3.Department of BiologyCalifornia State UniversityNorthridgeUSA
  4. 4.Institut de Ciències del MarConsejo Superior de Investigaciones CientíficasBarcelonaSpain

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