Estimations of free fatty acids (FFA) as a reliable proxy for larval performance in Mediterranean octocoral species

Published: Mar 3, 2022
Updated: 2022-03-03
Εenergy consumption gorgonians fatty acids octocorals.

The survival, behavior, and competence period of lecithotrophic larvae depends not only on the energy allocation transferred by maternal colonies, but also on the amount of energy consumed to sustain embryonic, larval, and post-larval development. The objective of the present work is to understand the effect of energy consumption on the performance of lecithotrophic larvae. To this aim, we analysed free fatty acid (FFA) content and composition of the larvae of three Mediterranean octocorals (Corallium rubrum, Eunicella singularis, and Paramuricea clavata) as a proxy for energy consumption. Results showed that C. rubrum larvae consume more FFA than P. clavata, whereas the energy consumed by E. singularis larvae is high but highly variable. These results are in accordance with the larval behavior of these three species, since C. rubrum larvae are characterized by their high swimming activity frequency, P. clavata larvae are almost inactive, and the swimming activity frequency of E. singularis larvae is high, although variable. The differences in FFA composition of the larvae suggest contrasting energetic strategies that could explain the differences in survival and recruitment rates. In fact, high dispersal and recruitment capacities for E. singularis larvae can be inferred from the FFA composition, whereas the high spatial and temporal variability of recruitment observed in C. rubrum may be related to the non-selective transfer of fatty acid (FA) from maternal colonies. Finally, the high recovery rates after mass mortality events observed in P. clavata could be favored by the presence of a specific FA [22:6(n-3)] related to adaptation mechanisms under environmental stresses during the first developmental stages.

Article Details
  • Section
  • Research Article
Download data is not yet available.
Author Biographies
NÚRIA VILADRICH, Universitat Autònoma de Barcelona

Institut de Ciència i Tecnologia Ambientals (Universitat Autònoma de Barcelona), Edifici Z Campus UAB,
Cerdanyola del Vallès, 08193, Spain & Sorbonne Université, CNRS, Laboratoire d’Ecogéochimie des Environnements Benthiques, LECOB, 66500 Banyuls-sur-Mer, France


California State University, Northridge, USA


Institut de Ciència i Tecnologia Ambientals (Universitat Autònoma de Barcelona), Edifici Z Campus UAB,
Cerdanyola del Vallès, 08193, Spain & Dipartimento di Scienze della Vita e dell’Ambiente (DiSVA), Università Politecnica delle Marche, 60131, Ancona, Italy


Institut de Ciències del Mar (ICM-CSIC), Barcelona, Spain; Instituto de Investigação em Ciências do Mar - Okeanos, Universidade dos Açores, Horta, Portugal


Sorbonne Université, CNRS, Laboratoire d’Ecogéochimie des Environnements Benthiques, LECOB, 66500 Banyuls-sur-Mer, France


Institut de Ciència i Tecnologia Ambientals (Universitat Autònoma de Barcelona), Edifici Z Campus UAB,
Cerdanyola del Vallès, 08193, Spain & DiSTeBA, Università del Salento, Lecce 73100, Italy; Instituto de Ciéncias do Mar (Labomar), Universidade Federal do Ceará, Fortaleza, Ceará, Brazil

Adjeroud, M., Kayal, M., Penin, L., 2017. Importance of recruitment processes in the dynamics and resilience of coral reef assemblages. p. 549-570. In: Marine Animal Forests: the ecology of benthic biodiversity hotspots. Rossi S, Bramanti L, Gori A, Orejas C (Eds). Springer, Germany.
Albessard, E., Mayzaud, P., Cuzin-Roudy, J., 2001. Variation of lipid classes among organs of the northern krill Meganyctiphanes norvegica, with respect to reproduction. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 129 (2-3), 373-390.
Arai, I., Kato, M., Heyward, A., Ikeda, Y., Iizuka, T. et al., 1993. Lipid composition of positively buoyant eggs of reef building corals. Coral Reefs, 12 (2), 71-75.
Bell, M.V., Sargent, J.R., 1996. Lipid nutrition and fish recruitment. Marine Ecology Progress Series, 134, 315-316.
Ben-David-Zaslow, R., Benayahu, Y., 1998. Competence and longevity in planulae of several species of soft corals. Marine Ecology Progress Series, 163, 235-243.
Bergé, J.P., Barnathan, G., 2005. Fatty acids from lipids of marine organisms: molecular biodiversity, roles as biomarkers, biologically active compounds, and economical aspects. Marine Biotechnology I, 96, 49-125.
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. Journal of Experimental Marine Biology and Ecology, 314 (1), 69-78.
Bransden, M.P., Battaglene, S.C., Morehead, D.T., Dunstan, G.A., Nichols, P.D., 2005. Effect of dietary 22:6n-3 on growth, survival and tissue fatty acid profile of striped trumpeter (Latris lineata) larvae fed enriched Artemia. Aquaculture, 243 (1-4), 331-344.
Chambers, J.M., Hastie, T.J. (Eds), 1992. Statistical models in S. Wadsworth and Brooks/Cole, Pacific Grove, California, 32pp. Chapelle, S., 1986. Aspects of phospholipid metabolism in crustaceans as related to changes in environmental temperatures and salinities. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 84 (4), 423-439.
Coma, R., Zabala, M., Gili, J.M., 1995. Sexual reproductive effort in the Mediterranean gorgonian Paramuricea clavata. Marine Ecology Progress Series, 117 (1-3), 185-192.
Coma, R., Linares, C., Ribes, M., Diaz, D., Garrabou, J. et al., 2006. Consequences of a mass mortality event on the populations of the gorgonian Eunicella singularis (Cnidaria: Octocorallia) in Menorca (Balearic Islands, NW Mediterranean). Marine Ecology Progress Series, 327, 51-60.
Conlan, J.A., Humphrey, C.A., Severati, A., Francis, D.S., 2017. Influence of different feeding regimes on the survival, growth, and biochemical composition of Acropora coral recruits. PloS one, 12 (11), e0188568.
Copeman, L.A., Parrish, C.C., Brown, J.A., Harel, M., 2002. Effects of docosahexanoic, eicosapentaenoic, and arachidonic acids on the growth, survival, lipid composition and pigmentation of yellowtail flounder (Limanda ferruginea): a live food enrichment experiment. Aquaculture, 210 (1-4), 285-304.
Costantini, F., Gori, A., Lopez-González, P., Bramanti, L., Rossi, S. et al., 2016. Limited genetic connectivity between gorgonian morphotypes along a depth gradient. PloS ONE, 11 (8), e0160678
Cupido, R., Cocito, S., Barsanti, M., Sgorbini, S., Peirano, A. et al., 2009. Unexpected long-term population dynamics in a canopy-forming gorgonian following mass mortality. Marine Ecology Progress Series, 394, 195-200.
da Costa, F., Nóvoa, S., Ojea, J., Martínez-Patiño, D., 2011. Changes in biochemical and fatty acid composition of the razor clam Solen marginatus (Solenidae: Bivalvia) during larval development. Marine Biology, 158 (8), 1829-1840.
Dalsgaard, J., St John, M., Kattner, G., Muller-Navarra, D., Hagen, W., 2003. Fatty acid trophic markers in the pelagic marine environment. Advanced Marine Biology, 46, 225-340.
DeMott, W.R., Muller-Navarra, D.C., 1997. The importance of highly unsaturated fatty acids in zooplankton nutrition: evidence from experiments with Daphnia, a cynaobacterium and lipid emulsions. Freshwater Biology, 38 (3), 649-664.
Dratz, E.A., Holte, L.L., 1992. The molecular spring model for the function of docosahexaenoic acid (22: 6w3) in biological membranes. p. 122-127. In: Essential fatty acids and eicosanoids. Sinclair, A., Gibson, R. (Eds). American Oil Chemists Society, Columbus, OH.
Dunstan, P.K., Johnson, C.R., 1998. Spatio-temporal variation in coral recruitment at different scales on Heron Reef, southern Great Barrier Reef. Coral Reefs, 17 (1), 71-81.
Fahl, K., Kattner, G., 1993. Lipid content and fatty acid composition of algal communities in sea-ice and water from the Weddell Sea (Antarctica). Polar Biology, 13 (6), 405-409.
Figueiredo, J., Baird, A., Cohen, M., Flot, J.F., Kamiki, T. et al., 2012. Ontogenetic change in the lipid and fatty acid composition of scleractinian coral larvae. Coral Reefs, 31 (2), 613-619.
Forcioli, D., Merle, P.L., Caligara, C., Ciosi, M., Muti, C. et al., 2011. Symbiont diversity is not involved in depth acclimation in the Mediterranean Sea whip Eunicella singularis. Marine Ecology Progress Series, 439, 57-71.
Gaither, M.R., Rowan, R., 2010. Zooxanthellar symbiosis in planula larvae of the coral Pocillopora damicornis. Journal of Experimental Marine Biology and Ecology, 386 (1-2), 45-53.
Gallager, S.M., Mann, R., 1986. Growth and survival of larvae of Mercenaria mercenaria (L.) and Crassostrea virginica (Gmelin) relative to broodstock conditioning and lipid content of eggs. Aquaculture, 56 (2), 105-121.
Garrabou, J., Harmelin, J.G., 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. Journal of Animal Ecology, 71 (6), 966-978.
Gili, J.M., Coma, R., 1998. Benthic suspension feeders: their paramount role in littoral marine food webs. Trends in Ecology & Evolution, 13 (8), 316-321. 122 Medit. Mar. Sci., 23/1 2022, 115-124
Grinyó, J., Viladrich, N., Díaz, D., Muñoz, A., Mallol, S. et al., 2018. Reproduction, energy storage and metabolic requirements in a mesophotic population of the gorgonian. Paramuricea macrospina. PloS ONE, 13 (9), e0203308.
Guizien, K., Viladrich, N., Martínez-Quintana, Á., Bramanti, L., 2020. Survive or swim: different relationships between migration potential and larval size in three sympatric Mediterranean octocorals. Scientific Report, 10, 18096.
Gurr, M.I., Harwood, J.L., Frayn, K.N. (Eds), 2002. Lipid biochemistry. Blackwell Science, Oxford, 248 pp.
Hall, J.M., Parrish, C.C., Thompson, R.J., 2000. Importance of unsaturated fatty acids in regulating bivalve and finfish membrane fluidity in response to changes in environmental temperature. p. 435-448. In: Seafood in health and nutrition. Shahidi, F. (Ed.). ScienceTech Publishing, St. John’s, Canada.
Harii, S., Yamamoto, M., Hoegh-Guldberg, O., 2010. The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals. Marine Biology, 157 (6), 1215-1224.
Harland, A.D., Navarro, J.C., Spencer-Davies, P., Fixter, L.M., 1993. Lipids of some Caribbean and Red Sea corals: total lipid, wax esters, triglycerides and fatty acids. Marine Biology, 117 (1), 113-117.
Holland, D.L., Spencer, B.E., 1973. Biochemical changes in fed and starved oysters, Ostrea edulis L. during larval development, metamorphosis and early spat growth. Journal of the Marine Biological Association of the United Kingdom, 53 (2), 287-298.
Imbs, A.B., 2013. Fatty acids and other lipids of corals: composition, distribution, and biosynthesis. Russian Journal of Marine Biology, 39 (3), 153-168.
Izquierdo, M.S., 1996. Essential fatty acid requirements of cultured marine fish larvae. Aquaculture Nutrition, 2 (4), 183-191.
Jonsson, P.R., Berntsson, K.M., André, C., Wängberg, S.A., 1999. Larval growth and settlement of the European oyster (Ostrea edulis) as a function of food quality measured as fatty acid composition. Marine Biology, 134 (3), 559-570.
Kahng, S.E., Benayahu, Y., Lasker, H.R., 2011. Sexual reproduction in octocorals. Marine Ecology Progress Series, 443, 265-283.
Kneeland, J., Hughen, K., Cervino, J., Hauff, B., Eglinton, T., 2013. Lipid biomarkers in Symbiodinium dinoflagellates: new indicators of thermal stress. Coral Reefs, 32 (4), 923- 934.
Kopp, C., Domart-Coulon, I., Barthelemy, D., Meibom, A., 2016. Nutritional input from dinoflagellate symbionts in reef-building corals is minimal during planula larval life stage. Science Advances, 2 (3), e1500681.
LaJeunesse, T.C., Parkinson, J.E., Gabrielson, P.W., Jeong, H.J., Reimer, J.D. et al., 2018. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Current Biology, 28 (16), 2570-2580.
Lasker, H.R., 1990. Clonal propagation and population dynamics of a gorgonian coral. Ecology, 71 (4), 1578-1589.
Latyshev, N.A., Naumenko, N.V., Svetashev, V.I., Latypov, Y.Y., 1991. Fatty acids of reef-building corals. Marine Ecology Progress Series, 76 (3), 295-301.
Linares, C., Coma, R., Mariani, S., Díaz, D., Hereu, B. et al., 2008. Early life history of the Mediterranean gorgonian Paramuricea clavata: implications for population dynamics. Invertebrate Biology, 127 (1), 1-11.
Linares, C., Cebrian, E., Coma, R., 2012. Effects of turf algae on recruitment and juvenile survival of gorgonian corals. Marine Ecology Progress Series, 452, 81-88.
Martínez-Quintana, A., Bramanti, L., Viladrich, N., Rossi, S., Guizien, K., 2015. Quantification of larval traits driving connectivity: the case of Corallium rubrum (L. 1758). Marine Biology, 162 (2), 309-318.
Mazorra, C., Bruce, M., Bell, J.G., Davie, A., Alorend, E. et al., 2003. Dietary lipid enhancement of broodstock reproductive performance and egg and larval quality in Atlantic halibut (Hippoglossus hippoglossus). Aquaculture, 227 (1- 4), 21-33.
Mies, M., Chaves-Filho, A.B., Miyamoto, S., Güth, A.Z., Tenório, A.A. et al., 2017. Production of three symbiosis- related fatty acids by Symbiodinium types in clades A–F associated with marine invertebrate larvae. Coral Reefs, 36 (4), 1319-1328.
Nenadic, O., Greenacre, M., 2007. Correspondence Analysis in R, with two- and three-dimensional graphics: The ca package. Journal of Statistical Software, 20 (3), 1-3.
Okubo, N., Yamamoto, H.H., Nakaya, F., Okaji, K., 2008. Oxygen consumption of a single embryo/planula in the reef-building coral Acropora intermedia. Marine Ecology Progress Series, 366, 305-309.
Padrón, M., Costantini, F., Baksay, S., Bramanti, L., Guizien, K., 2018. Passive larval transport explains recent gene flow in a Mediterranean gorgonian. Coral Reefs, 37 (2), 495-506.
Papina, M., Meziane, T., van Woesik, R., 2003. Symbiotic zooxanthellae provide the host-coral Montipora digitata with polyunsaturated fatty acids. Comparative Biochemistry and Physiology, 135, 533-537.
Pawlik, J.R., Faulkner, D.J., 1986. Specific free fatty acids induce larval settlement and metamorphosis of the reef-building tube worm Phragmatopoma califomica (Fewkes). Journal of Experimental Marine Biology and Ecology, 102 (2-3), 301-310.
Pechenik, J.A., 1990. Delayed metamorphosis by larvae of benthic marine-invertebrates - does it occur? Is there a price to pay? Ophelia, 32 (1-2), 63-94.
Pond, D.W., Harris, R., Head, R., Harbour, D., 1996. Environmental and nutritional factors determining seasonal variability in the fecundity and egg viability of Calanus helgolandicus in coastal waters off Plymouth, UK. Marine Ecology Progress Series, 143, 45-63.
Pupier, C.A., Mies, M., Fine, M., Bastos Francini‐Filho, R., Pereira Brandini F. et al., 2021. Lipid biomarkers reveal the trophic plasticity of octocorals along a depth gradient. Limnology and Oceanography, 66 (5), 2078-2087.
Qian, P.Y., Chia, F.S., 1991. Fecundity and egg size were mediated by quality of diet in the marine polychaete worm, Capitella sp. Journal of Experimental Marine Biology and Ecology, 148 (1), 11-25.
Qian, P.Y., McEdward, L.R., Chia, F.S., 1990. Effects of delayed settlement on survival, growth, and reproduction in the spionid polychaete, Polydora ligni. Invertebrate Reproduction & Development, 18 (3), 147-152.
Radice, V.Z., Brett, M.T., Fry, B., Fox, M.D., Hoegh-Guldberg, Medit. Mar. Sci., 23/1 2022, 115-124 123 O. et al., 2019. Evaluating coral trophic strategies using fatty acid composition and indices. PloS ONE, 14 (9), e0222327.
Rainuzzo, J.R., Reitan, K.I., Jørgensen, L., Olsen, Y., 1994. Lipid composition in turbot larvae fed live feed cultured by emulsions of different lipid classes. Comparative Biochemistry and Physiology Part A: Physiology, 107 (4), 699-710.
Ribes, M., Coma, R., Rossi, S., Michelli, M., 2007. The cycle of gonadal development of Eunicella singularis (Cnidaria: Octocorallia). Invertebrate Biology, 126 (4), 307-317.
Richmond, R.H., 1987. Energetic relationships and biogeographical differences among fecundity, growth and reproduction in the reef coral Pocillopora damicornis. Bulletin of Marine Science, 41 (2), 594-604.
Rossi, S., 2013. The destruction of the “animal forests” in the oceans: Towards an over-simplification of the benthic ecosystems. Ocean & Coastal Management, 84, 77-85.
Rossi, S., Tsounis, G., 2007. Temporal and spatial variation in protein, carbohydrate, and lipid levels in Corallium rubrum (Anthozoa, Octocorallia). Marine Biology, 152 (2), 429-439.
Rossi, S., Sabatés, A., Latasa, M., Reyes, E., 2006. Lipid biomarkers and trophic linkages between phytoplankton, zooplankton and anchovy (Engraulis encrasicolus) larvae in the NW Mediterranean. Journal of Plankton Research, 28 (6), 551-562.
Roth, M.S., Fan, T.Y., Deheyn, D.D., 2013. Life history changes in coral fluorescence and the effects of light intensity on larval physiology and settlement in Seriatopora hystrix. PLoS ONE, 8 (3), e59476.
Santangelo, G., Maggi, E., Bramanti, L., Bongiorni, L., 2003. Demography of the over-exploited Mediterranean red coral (Corallium rubrum L. 1758). Scientia Marina, 68, 199-204.
Santangelo, G., Bramanti, L., Rossi, S., Tsounis, G., Vielmini, I. et al., 2012. Patterns of variation in recruitment and post-recruitment processes of the Mediterranean precious gorgonian coral Corallium rubrum. Journal of Experimental Marine Biology and Ecology, 411, 7-13.
Santangelo, G., Cupido, R., Cocito, S., Bramanti, L., Priori, C. et al., 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 (1), 171-187.
Sargent, J.R., McEvoy, L.A., Bell, J.G., 1997. Requirements, presentation, and sources of polyunsaturated fatty acids in marine fish larval feeds. Aquaculture, 155 (1-4), 117-127.
Sargent, J.R., Parks, R.J., Mueller-Harvey, I., Henderson, R.J., 1988. Lipid biomarkers in marine ecology. p. 119-138. In: Microbes in the sea. Sliegh, M.A. (Ed.). Ellis Horwood Ltd, Chichester.
Sargent, J.R., McEvoy, L.A., Estevez, A., Bell, J.G., Bell, M. et al., 1999. Lipid nutrition of marine fish during early development: current status and future directions. Aquaculture, 179 (1-4), 217-229.
Schultz, D.M., Quinn, J.G., 1973. Fatty acid composition of organic detritus from Spartina alterniflora. Estuarine and Coastal Marine Science, 1 (2), 177-190.
Tocher, D.R., 2003. Metabolism and functions of lipids and fatty acids in teleost fish. Reviews in Fisheries Science, 11 (2), 107-184.
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. Limnology Oceanography, 53, 2702-2710.
Tsounis, G., Rossi, S., Laudien, J., Bramanti, L., Fernández, N. et al., 2006. Diet and seasonal prey capture rate in the Mediterranean red coral (Corallium rubrum L.). Marine Biology, 149 (2), 313-325.
Velásquez, J., Sánchez, J.A., 2015. Octocoral species assembly and coexistence in Caribbean coral reefs. PloS ONE, 10 (7), e0129609.
Viladrich, N., Bramanti, L., Tsounis, G., Chocarro, B., Martínez-Quitana, Á. et al., 2016. Variations of lipid and free fatty acid contents during spawning in two temperate octocorals with different reproductive strategies: surface versus internal brooder. Coral Reefs, 35 (3), 1033-1045.
Viladrich, N., Bramanti, L., Tsounis, G., Martínez-Quintana, A., Ferrier-Pagès, C. et al., 2017. Variation of lipid and free fatty acid contents during larval release in two temperate octocorals according to their trophic strategy. Marine Ecology Progress Series, 573, 117-128.
Volkman, J.K., Jeffrey, S.W., Nichols, P.D., Rogers, G.I., Garland, C.D., 1989. Fatty acid and lipid composition of 10 species of microalgae used in mariculture. Journal of Experimental Marine Biology and Ecology, 128 (3), 219-240.
Weinberg, S., 1979a. Autecology of shallow-water Octocorallia from Mediterranean rocky substrata, I. The Banyuls area. Bijdragen tot de Dierkunde, 49 (1), 1-15.
Weinberg, S., 1979b. The light-dependent behaviour of planula larvae of Eunicella singularis and Corallium rubrum and its implication for octocorallian ecology. Bijdragen tot de Dierkunde, 49 (1), 16-30.
Weinberg, S., Weinberg, F., 1979. The life cycle of a Gorgonian: Eunicella singularis (Esper, 1794). Bijdragen tot de Dierkunde, 48 (2), 127-140.
Wen, X.B., Chen, L.Q., Zhou, Z.L., Ai, C.X., Deng, G.Y., 2002. Reproduction response of Chinese mitten-handed crab (Eriocheir sinensis) fed different sources of dietary lipid. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 131 (3), 675-681.
Wild, C., Hoegh-Guldberg, O., Naumann, M.S., Colombo-Pallotta, M.F., Ateweberhan, M. et al., 2011. Climate change impedes scleractinian corals as primary reef ecosystem engineers. Marine and Freshwater Research, 62 (2), 205-215.
Yakovleva, I.M., Baird, A.H., Yamamoto, H.H., Bhagooli, R., Nonaka, M. Hidaka, M., 2009. Algal symbionts increase oxidative damage and death in coral larvae at high temperatures. Marine Ecology Progress Series, 378, 105-112.
Yoshioka, P.M., 1996. Variable recruitment and its effects on the population and community structure of shallow-water gorgonians. Bulletin of Marine Science, 59 (2), 433-443.
Zelli, E., Quéré, G., Lago, N., Di Franco, G., Costantini, F. et al., 2020. Settlement dynamics and recruitment responses of Mediterranean gorgonians larvae to different crustose coralline algae species. Journal of Experimental Marine Biology and Ecology, 530, 151427.
Most read articles by the same author(s)