Abstract
Scleractinian cold-water corals (CWC) act as key ecosystem engineers in deep-sea reef environments worldwide. However, our current understanding of their trophic ecology is still limited, particularly in understudied temperate oceanic regions such as the Mediterranean Sea. Hence, this study investigated the trophic ecology of the CWC Desmophyllum dianthus and Madrepora oculata by employing lipid biomarker techniques and compound-specific isotope analyses on coral tissues, suspended particulate organic matter (sPOM), and surface sediment sampled in a Mediterranean CWC habitat. CWC exhibited high contents of poly- and monounsaturated fatty acids (FA) (≥49 and 32 % of FA, respectively) and cholesterol (≥67 % of sterols), while sPOM and sediment samples were enriched in saturated FA (≥44 % of FA) and sitosterol (≥35 % of sterols). CWC contained some rare very long-chained polyunsaturated FA (>C22) and ergosterol absent in sPOM and sediment samples. Our results indicate that Mediterranean CWC mainly consume living food items, rather than detrital sPOM or resuspended sediment, and provide evidence for preferred feeding on omnivorous and carnivorous zooplankton. Overall, these findings provide new insights to the trophic ecology of two common CWC from the Mediterranean Sea.
References
Arts MT, Brett MT, Kainz MJ (2009) Lipids in aquatic ecosystems. Springer, New York
Bachok Z, Mfilinge P, Tsuchiya M (2006) Characterization of fatty acid composition in healthy and bleached corals from Okinawa, Japan. Coral Reefs 25:545–554
Barrett SM, Volkman JK, Dunstan GA, Leroi JM (1995) Sterols of fourteen species of marine diatoms (Bacillariophyta). J Phycol 31:360–369
Bosc E, Bricaud A, Antoine D (2004) Seasonal and interannual variability in algal biomass and primary production in the Mediterranean Sea, as derived from 4 years of SeaWiFS observations. Global Biogeochem Cycles 18:GB1005
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
Chikaraishi Y, Naraoka H (2003) Compound-specific δ13C analyses of n-alkanes extracted from terrestrial and aquatic plants. Phytochemistry 63:361–371
Cossins AR, Prosser CL (1978) Evolutionary adaptation of membranes to temperature. Proc Nat Am Soc 75:2040–2043
Dalsgaard J, St John M, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340
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
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 277:13–23
Fauland A, Köfeler H, Trötzmüller M, Knopf A, Hartler J, Eberl A, Chitraju C, Lankmayr E, Spener F (2011) A comprehensive method for lipid profiling by liquid chromatography-ion cyclotron resonance mass spectrometry. J Lipid Res 52:2314–2322
Ghisolfi J, Putet G (1992) Essential fatty acids and infant nutrition. John Libbey Eurotext, Paris, p 185
Grimalt JO, Albaigés J (1990) Characterization of the depositional environments of the Ebro Delta (western Mediterranean) by the study of sedimentary lipid markers. Mar Geol 95:207–224
Heffernan AL, Aylward LL, Toms LML, Sly PD, Macleod M, Mueller JF (2014) Pooled biological specimens for human biomonitoring of environmental chemicals: opportunities and limitations. J Expo Sci Environ Epidemiol 24:225–232
Hofmann M, Eichenberger W (1997) Lipids and fatty acid composition of the marine brown algae Dictyopteris membranaceae. Plant Cell Physiol 38:1046–1052
Kattner G, Krause M, Trahms J (1981) Lipid composition of some typical North Sea copepods. Mar Ecol Prog Ser 4:69–74
Kiriakoulakis K, White M, Bett BJ, Wolff GA (2004) Organic biogeochemistry of the Darwin Mounds, a deep-water coral ecosystem, of the NE Atlantic. Deep Sea Res Part 1 Oceanogr Res Pap 51:1937–1954
Kiriakoulakis K, Fischer E, Wolff GA, Freiwald A, GrehanA Roberts JM (2005) Lipids and nitrogen isotopes of two deep-water corals from the North-East Atlantic: initial results and implications for their nutrition. In: Freiwald A, Roberts JM (eds) Cold water corals and ecosystems. Springer, Berlin, pp 715–729
Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273–306
Maier C, Watremez P, Taviani M, Weinbauer MG, Gattuso JP (2011) Calcification rates and the effect of ocean acidification on Mediterranean cold-water corals. Proc R Soc Lond B Biol Sci 279:1716–1723
Mancini I, Guerriero A, Guella G, Bakken T, Zibrowius H, Pietra F (1999) Novel 10-hydroxydocosapolyenoic acids from deep-water scleractinian corals. Helvetica Chimica Acta 82:677–684
Mazzocchi MG, Nervegna D, D’Elia G, Di Capua I, Aguzzi L, Boldrin A (2003) Spring mesozooplankton communities in the epipelagic Ionian Sea in relation to the Eastern Mediterranean Transient. J Geophys Res 108:8114
Mortensen PB, Hovland MT, Fosså JH, Furevik DM (2001) Distribution, abundance and size of Lophelia pertusa coral reefs in mid-Norway in relation to seabed characteristics. J Mar Biol Assoc UK 81:581–597
Mueller CE, Larsson AI, Veuger B, Middelburg JJ, van Oevelen D (2014) Opportunistic feeding on various organic food sources by the cold-water coral Lophelia pertusa. Biogeosciences 11:123–133
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
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
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
Nes WR, McKean ML (1977) Biochemistry of steroids and other isopentenoids. University Park Press, Baltimore
Ohman MD (1996) Freezing and storage of copepod samples for the analysis of lipids. Mar Ecol Prog Ser 130:295–298
Orejas C, Gori A, Lo Iacono C, Puig P, Gili JM, Dale MRT (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
Pires DO, Silva JC, Bastos ND (2014) Reproduction of deep-sea reef-building corals from the southwestern Atlantic. Deep Sea Res Part 2 Top Stud Oceanogr 99:51–63
Planque B, Batten S (2000) Calanus finmarchicus in the North Atlantic: the year of Calanus in the context of interdecadal change. ICES J Mar Sci 57:1528–1535
Poulos A (1995) Very long chain fatty acids in higher animals - A review. Lipids 30:1–14
Rielley G, Collier RJ, Jones DM, Eglinton G (1991) The biogeochemistry of Ellesmere Lake, U.K. I: source correlation of leaf wax inputs to the sedimentary lipid record. Org Geochem 17:901–912
Roberts JM, Wheeler AJ, Freiwald A (2006) Reefs of the deep: the biology and geology of cold-water coral ecosystems. Science 312:543–547
Roberts JM, Wheeler AJ, Freiwald A, Cairns S (2009) Cold-water corals: the biology and geology of deep-sea coral habitats. Cambridge University Press, Cambridge
Robinson AJ, Richards WG, Thomas PJ, Hann MM (1994) Head group and chain behavior in biological membranes: a molecular dynamics computer simulation. Biophys J 67:2345–2354
Schembri PJ, Dimech M, Camilleri M, Page R (2007) Living deep-water Lophelia and Madrepora corals in Maltese waters (Strait of Sicily, Mediterranean Sea). Cah Biol Mar 48:77–83
Taviani M, Freiwald A, Zibrowius H (2005) Deep-coral growth in the Mediterranean Sea: an overview. In: Freiwald A, Roberts JM (eds) Cold water corals and ecosystems. Springer, Berlin, pp 137–156
Taviani M, Angeletti L, Antolini B, Ceregato A, Froglia C, Lopez Correa M, Montagna P, Remia A, Trincardi F, Vertino A (2011) Geo-biology of Mediterranean deep-water coral ecosystems. In: Brugnoli E (ed) Marine Research at CNR, Volume DTA 6:705–719
Thiem Ø, Ravagnan E, Fosså JH, Berntsen J (2006) Food supply mechanisms for cold-water corals along a continental shelf edge. J Mar Syst 26:1481–1495
Tolosa I, de Mora S (2004) Isolation of neutral and acidic lipid biomarker classes for compound-specific-carbon isotope analysis by means of solvent extraction and normal-phase high-performance liquid chromatography. J Chromatogr A 1045:71–84
Tolosa I, Treignier C, Grover R, Ferrier-Pagès C (2011) Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids, sterols, and alcohols in the scleractinian coral Turbinaria reniformis. Coral Reefs 30:763–774
Tolosa I, Fiorini S, Gasser B, Martin J, Miquel JC (2013) Carbon sources in suspended particles and surface sediments from the Beaufort Sea revealed by molecular lipid biomarkers and compound-specific isotope analysis. Biogeosciences 10:2061–2087
Tolosa I, Vescovali I, LeBlond N, Marty JC, de Mora S, Prieur L (2004) Distribution of pigments and fatty acid biomarkers in particulate matter from the frontal structure of the Alboran Sea (SW Mediterranean Sea). Mar Chem 88:103–125
Treignier C, Grover R, Ferrier-Pagès C, Tolosa I (2008) Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis. Limnol Oceanogr 53:2702–2710
Treignier C, Tolosa I, Grover R, Reynaud S, Ferrier-Pagès C (2009) Carbon isotope composition of fatty acids and sterols in the scleractinian coral Turbinaria reniformis: Effect of light and feeding. Limnol Oceanogr 54:1933–1940
Volkman JK, Johns RB, Gillan FT, Perry GJ, Bavor HJ Jr (1980) Microbial lipids of an intertidal sediment I. Fatty acids and hydrocarbons. Geochim Cosmochim Acta 44:1133–1143
Volkman JK, Barrett SM, Blackburn SI, Mansour MP, Sikes EL, Gelin F (1998) Microalgal biomarkers: a review of recent research developments. Org Geochem 29:1163–1179
Waller RG, Tyler PA (2005) The reproductive biology of two deep-water, reef-building scleractinians from the NE Atlantic Ocean. Coral Reefs 24:514–522
Yamashiro H, Oku H, Higa H, Chinen I, Sakai K (1999) Composition of lipids, fatty acids and sterols in Okinawan corals. Comp Biochem and Physiol 122:397–407
Acknowledgments
This research was supported by the Prince Albert II Foundation (COMP project), the IAEA and the government of the Principality of Monaco. We are grateful to masters, crew, and colleagues on-board RV Urania during mission MEDCOR, with special thanks to C. Maier (LOV Villefranche) and L. Angeletti (ISMAR-CNR). Partial funding and ship time was provided by CNR, the FP-VII collaborative projects HERMIONE (Contract Number 226354), and COCONET (Grant Agreement No. 287844) of the European Commission; this research contributes to RITMARE project. This is ISMAR-Bologna Scientific Contribution Number 1805. The IAEA is grateful for the support provided to the Environment Laboratories by the Government of the Principality of Monaco. We thank the topic editor and four anonymous reviewers for their help in improving the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Ruth D. Gates
Renaud Grover and Christine Ferrier-Pagès have contributed equally to this work.
Rights and permissions
About this article
Cite this article
Naumann, M.S., Tolosa, I., Taviani, M. et al. Trophic ecology of two cold-water coral species from the Mediterranean Sea revealed by lipid biomarkers and compound-specific isotope analyses. Coral Reefs 34, 1165–1175 (2015). https://doi.org/10.1007/s00338-015-1325-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-015-1325-8