Journal of Applied Phycology

, Volume 28, Issue 3, pp 1975–1986 | Cite as

Settlement inhibition of marine biofilm bacteria and barnacle larvae by compounds isolated from the Mediterranean brown alga Taonia atomaria

  • Ahlem Othmani
  • Robert Bunet
  • Jean-Luc Bonnefont
  • Jean-François Briand
  • Gérald Culioli


The antifouling (AF) properties of phytochemicals isolated from the Mediterranean brown seaweed Taonia atomaria have been assayed against several colonizing organisms. Eight compounds were isolated and their chemical structures characterized by spectroscopic techniques (NMR, MS) and comparison with literature data. The phytochemical composition of the extracts of T. atomaria was found to be mainly attributable to sesquiterpenes. Accordingly, a new germacrane, germacra-4(15),5,10(14)-trien-9-ol (1), is described together with five other sesquiterpenoids (-)-gleenol (2); α-cadinol methyl ether (3), (-)-trans-calamenene (4), (1S, 5E, 7S) 1-acetoxygermacra-4(15),5,10(14)-triene (5), and 4-peroxymuurol-5-ene (6). Moreover, two lipidic compounds, a polyunsaturated fatty acid, (5Z, 8Z, 11Z, 14Z, 17Z)-eicosa-5,8,11,14,17-pentaenoic acid (7), and a glycerol derivative, sn-3-O-(geranylgeranyl)glycerol (8), were also isolated. The known compounds 3, 67 are described here for the first time from this alga. In comparison with commercial antifoulants [tributyltin oxide (TBTO), zineb, and copper pyrithione (CuPT)], compounds 1, 2, 4, 6, and 8 were evaluated for their toxicity and capacity to inhibit the settlement of five bacteria isolated from marine biofilms. Toxicity and anti-settlement activity of 1, 2, and 6 were also assessed against two barnacle species (Amphibalanus amphitrite and Balanus perforatus). Regarding bacteria, a significant anti-adhesion effect was recorded for 8 (EC50 between 25 and 50 μM) with moderate associated toxicity. Considering the settlement inhibition of barnacle cyprids, (-)-gleenol (2) exhibited a strong AF efficacy (EC50 < 5 μM) with moderate toxicity. In addition, as B. perforatus showed similar responses to the reference A. amphitrite with all compounds, this species may be proposed as an alternative model for anti-macrofouling assessment, especially in temperate areas. Overall, these results suggest that a number of the tested compounds could, alone or in combination, play a critical role in limiting the fouling at the T. atomaria surface.


Antifouling Algal metabolite Biofilm-forming bacteria Anti-adhesion Toxicity Barnacles 



This work was financially supported by the Ministry of Higher Education and Scientific Research of Tunisia (A.O. PhD grant). Special thanks are given to Pr. O. De Clerck (Ghent University) for taxonomic identification of the algal material, and to C. Compère (IFREMER, Brest, France) and D. Haras (LBCM, Université de Bretagne Sud, France) for the supply of the D41 and 4M6 strains, respectively. The authors also would like to thank P. Aublanc, D. Kirchhofer, and T. Miard (Institut Océanographique Paul Ricard, France) for technical assistance.

Supplementary material

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ESM 1 (PDF 1578 kb)


  1. Abatis D, Vagias C, Galanakis D, Norris JN, Moreau D, Roussakis C, Roussis V (2005) Atomarianones A and B: two cytotoxic meroditerpenes from the brown alga Taonia atomaria. Tetrahedron Lett 46:8525–8529CrossRefGoogle Scholar
  2. Amico V, Oriente G, Piattelli M, Tringali C, Fattorusso E, Magno S, Mayol L (1979) Sesquiterpenes based on the cadalane skeleton from the brown alga Dilophus fasciola. Experientia 35:450–451CrossRefGoogle Scholar
  3. Areche C, San-Martín A, Rovirosa J, Soto-Delgado J, Contreras R (2009) An unusual halogenated meroditerpenoid from Stypopodium flabelliforme: Studies by NMR spectroscopic and computational methods. Phytochemistry 72:1315–1320CrossRefGoogle Scholar
  4. Blay G, Collado AM, García B, Pedro JR (2005) Silicon guided rearrangement of epoxydecalines to spirocyclic compounds. Synthesis of gleenol and axenol from carvone. Tetrahedron 61:10853–10860CrossRefGoogle Scholar
  5. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2014) Marine natural products. Nat Prod Rep 31:160–258, and previous reports in the seriesCrossRefPubMedGoogle Scholar
  6. Briand J-F (2009) Marine antifouling laboratory bioassays: an overview of their diversity. Biofouling 25:297–311CrossRefPubMedGoogle Scholar
  7. Brian-Jaisson F, Ortalo-Magné A, Guentas-Dombrowsky L, Armougom F, Blache Y, Molmeret M (2014) Identification of bacterial strains isolated from the Mediterranean sea exhibiting different abilities of biofilm formation. Microb Ecol 68:94–110CrossRefPubMedGoogle Scholar
  8. Camps M, Briand J-F, Guentas-Dombrowsky L, Culioli G, Bazire A, Blache Y (2011) Antifouling activity of commercial biocides vs. natural and natural-derived products assessed by marine bacteria adhesion bioassay. Mar Pollut Bull 62:1032–1040CrossRefPubMedGoogle Scholar
  9. Chakraborty K, Lipton AP, Paul Raj R, Vijayan KK (2010) Antibacterial labdane diterpenoids of Ulva fasciata Delile from southwestern coast of the Indian Peninsula. Food Chem 119:1399–1408CrossRefGoogle Scholar
  10. Changyun W, Haiyan L, Changlun S, Yanan W, Liang L, Huashi G (2008) Chemical defensive substances of soft corals and gorgonians. Acta Ecol Sin 28:2320–2328CrossRefGoogle Scholar
  11. Clare AS, Aldred N (2009) Surface colonisation by marine organisms and its impact on antifouling research. IN Hellio C, Yebra D (eds) Advances in Marine Antifouling Coatings and Technologies. Woodhead Publishing. Pp 46-79Google Scholar
  12. Clare AS, Rittschof D, Gerhart DJ, Hooper GJ, Bonaventura J (1999) Antisettlement and narcotic action of analogues of diterpene marine natural product antifoulants from octocorals. Mar Biotechnol 1:427–436CrossRefPubMedGoogle Scholar
  13. Costlow JD Jr, Bookhout CG (1958) Larval development of Balanus amphitrite var. denticulata Broch reared in the laboratory. Biol Bull 114:284–295CrossRefGoogle Scholar
  14. da Gama BAP, Plouguerné E, Pereira RC (2014) The antifouling defence mechanisms of marine macroalgae. Adv Bot Res 71:413–440CrossRefGoogle Scholar
  15. Dafforn KA, Lewis JA, Johnston EL (2011) Antifouling strategies: History and regulation, ecological impacts and mitigation. Mar Pollut Bull 62:453–465CrossRefPubMedGoogle Scholar
  16. De Nys R, Dworjanyn SA, Steinberg PD (1998) A new method for determining surface concentrations of marine natural products on seaweeds. Mar Ecol Prog Ser 162:79–87CrossRefGoogle Scholar
  17. de Paula JC, Vallim MA, Teixeira VL (2011) What are and where are the bioactive terpenoids metabolites from Dictyotaceae (Phaeophyceae). Rev Bras Farmacogn 21:216–228CrossRefGoogle Scholar
  18. De Rosa S, De Giulio A, Iodice C, Zavodink N (1994) Sesquiterpenes from the brown alga Taonia atomaria. Phytochemistry 37:1327–1330CrossRefGoogle Scholar
  19. Dobretsov S, Abed RMM, Teplitski M (2013) Mini-review: Inhibition of biofouling by marine microorganisms. Biofouling 29:423–441CrossRefPubMedGoogle Scholar
  20. Dupré S, Grenz M, Jakupovic J, Bohlmann F, Niemeyer HM (1991) Eremophilane, germacrane and shikimic acid derivatives from chilean Senecio species. Phytochemistry 30:1211–1220CrossRefGoogle Scholar
  21. Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T (2013) The seaweed holobiont: understanding seaweed–bacteria interactions. FEMS Microbiol Rev 37:462–476CrossRefPubMedGoogle Scholar
  22. El Hattab M, Bouzidi N, Ortalo-Magné A, Daghbouche Y, Richou M, Chitour SE, de Reviers B, Piovetti L (2009) Eicosapentaenoic acid: Possible precursor of the phloroglucinol derivatives isolated from the brown alga Zonaria tournefortii (J.V. Lamouroux) Montagne. Biochem Syst Ecol 37:55–58CrossRefGoogle Scholar
  23. Faimali M, Sepcic K, Turk T, Geraci S (2003) Non-toxic antifouling activity of polymeric 3-alkylpyridinium salts from the Mediterranean sponge Reniera sarai (Pulitzer-Finali). Biofouling 19:47–56CrossRefPubMedGoogle Scholar
  24. Fattorusso E, Magno S, Mayol L, Amico V, Oriente G, Piattelli M, Tringali C (1978) Isolation of (2S,8R)-germacra-1(11),5(12), E6-trien-2-ol acetate from the brown alga Dilophus fasciola. Tetrahedron Lett 19:4149–4152CrossRefGoogle Scholar
  25. Fusetani N (2004) Biofouling and antifouling. Nat Prod Rep 21:94–104CrossRefPubMedGoogle Scholar
  26. Fusetani N (2011) Antifouling marine natural products. Nat Prod Rep 28:400–410CrossRefPubMedGoogle Scholar
  27. Gonzalez AG, Darias J, Martin JD (1971) Taondiol, a new component from Taonia atomaria. Tetrahedron Lett 12:2729–2732CrossRefGoogle Scholar
  28. Gonzalez AG, Darias J, Martin JD, Pascual C (1973) Marine natural products of the atlantic zone.V.The structure and chemistry of taondiol and related compounds. Tetrahedron 29:1605–1609CrossRefGoogle Scholar
  29. Gonzalez AG, Darias J, Martin JD, Norte M (1974) Atomaric acid, a new component from Taonia atomaria. Tetrahedron Lett 15:3951–3954CrossRefGoogle Scholar
  30. Grasland B, Mitalane J, Briandet R, Quémener E, Meylheuc T, Linossier I, Vallée-Réhel K, Haras D (2003) Bacterial biofilm in seawater: cell surface properties of early-attached marine bacteria. Biofouling 19:307–313CrossRefPubMedGoogle Scholar
  31. Guiry MD, Guiry GM (2014) AlgaeBase. World-wide electronic publication. National University of Ireland, GalwayGoogle Scholar
  32. Hanssen K, Cervin G, Trepos R, Petitbois J, Haug T, Hansen E, Andersen J, Pavia H, Hellio C, Svenson J (2014) The bromotyrosine derivative ianthelline isolated from the Arctic marine sponge Stryphnus fortis inhibits marine micro- and macrobiofouling. Mar Biotechnol 16:684–694CrossRefPubMedGoogle Scholar
  33. Harder T, Campbell A, Egan S, Steinberg P (2012) Chemical mediation of ternary interactions between marine holobionts and their environment as exemplified by the red alga Delisea pulchra. J Chem Ecol 38:442–450CrossRefPubMedGoogle Scholar
  34. Hiraga Y, Taino K, Kurokawa M, Takagi R, Ohkata K (1997) (−)-Loliolide and other germination inhibitory active constituents in Equisetum arvense. Nat Prod Lett 10:181–186CrossRefGoogle Scholar
  35. Hirota H, Tomono Y, Fusetani N (1996) Terpenoids with antifouling activity against barnacle larvae from the marine sponge Acanthella cavernosa. Tetrahedron 52:2359–2368CrossRefGoogle Scholar
  36. Konstantinou IK, Albanis TA (2004) Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review. Environ Internat 30:235–248CrossRefGoogle Scholar
  37. Lachnit T, Wahl M, Harder T (2010) Isolated thallus-associated compounds from the macroalga Fucus vesiculosus mediate bacterial surface colonization in the field similar to that on the natural alga. Biofouling 26:247–255CrossRefPubMedGoogle Scholar
  38. Lachnit T, Fischer M, Künzel S, Baines JF, Harder T (2013) Compounds associated with algal surfaces mediate epiphytic colonization of the marine macroalga Fucus vesiculosus. FEMS Microbiol Ecol 84:411–420CrossRefPubMedGoogle Scholar
  39. Lankadurai B, Wolfe D, Whitfield Åslund M, Simpson A, Simpson M (2013) 1H NMR-based metabolomic analysis of polar and non-polar earthworm metabolites after sub-lethal exposure to phenanthrene. Metabolomics 9:44–56CrossRefGoogle Scholar
  40. Leroy C, Delbarre-Ladrat C, Ghillebaert F, Rochet MJ, Compère C, Combes D (2007) A marine bacterial adhesion microplate test using the DAPI fluorescent dye: a new method to screen antifouling agents. Lett Appl Microbiol 44:372–378CrossRefPubMedGoogle Scholar
  41. Manzo S, Schiavo S, Aleksi P, Tabaku A (2014) Application of a toxicity test battery integrated index for a first screening of the ecotoxicological threat posed by ports and harbors in the southern Adriatic Sea (Italy). Environ Monit Assess 186:7127–7139CrossRefPubMedGoogle Scholar
  42. Maréchal J-P, Hellio C (2011) Antifouling activity against barnacle cypris larvae: Do target species matter (Amphibalanus amphitrite versus Semibalanus balanoides)? Int Biodeter Biodegr 65:92–101CrossRefGoogle Scholar
  43. Maximilien R, de Nys R, Holmström C, Gram L, Givskov M, Crass K, Kjelleberg S, Steinberg PD (1998) Chemical mediation of bacterial surface colonisation by secondary metabolites from the red alga Delisea pulchra. Aquat Microb Ecol 15:233–246CrossRefGoogle Scholar
  44. Mokrini R, Mesaoud MB, Daoudi M, Hellio C, Maréchal J-P, El Hattab M, Ortalo-Magné A, Piovetti L, Culioli G (2008) Meroditerpenoids and derivatives from the brown alga Cystoseira baccata and their antifouling properties. J Nat Prod 71:1806–1811CrossRefPubMedGoogle Scholar
  45. Nagashima F, Asakawa Y (2001) Sesqui- and diterpenoids from two Japanese and three European liverworts. Phytochemistry 56:347–352CrossRefPubMedGoogle Scholar
  46. Nagashima F, Toyota M, Asakawa Y (1990) Terpenoids from some Japanese liverworts. Phytochemistry 29:2169–2174CrossRefGoogle Scholar
  47. Nakashima K, Imoto M, Sono M, Tori M, Nagashima F, Asakawa Y (2002) Total synthesis of (-)-(7S,10R)-calamenene and (-)-(7S,10R)-2-hydroxycalamenene by use of a ring-closing metathesis reaction. A comparison of the cis- and trans-isomers. Molecules 7:517–527CrossRefGoogle Scholar
  48. Nakazaki A, Era T, Kobayashi S (2007) Total synthesis of (±)-gleenol and (±)-axenol via a functionalized spiro[4.5]decane. Chem Pharm Bull 55:1606–1609CrossRefPubMedGoogle Scholar
  49. Nogata Y, Yoshimura E, Shinshima K, Kitano Y, Sakaguchi I (2003) Antifouling substances against larvae of the barnacle Balanus amphitrite from the marine sponge, Acanthella cavernosa. Biofouling 19:193–196CrossRefPubMedGoogle Scholar
  50. Norms E, Crisp DJ (1953) The distribution and planktonic stages of the cirripede Balanus perforatus Bruguière. Proc Zool Soc Lond 123:393–409CrossRefGoogle Scholar
  51. Nylund GM, Gribben PE, De Nys R, Steinberg PD, Pavia H (2007) Surface chemistry versus whole-cell extracts: antifouling tests with seaweed metabolites. Mar Ecol Prog Ser 329:73–84CrossRefGoogle Scholar
  52. Nylund GM, Persson F, Lindegarth M, Cervin G, Hermansson M, Pavia H (2010) The red alga Bonnemaisonia asparagoides regulates epiphytic bacterial abundance and community composition by chemical defence. FEMS Microbiol Ecol 71:84–93CrossRefPubMedGoogle Scholar
  53. Nylund GM, Weinberger F, Rempt M, Pohnert G (2011) Metabolomic assessment of induced and activated chemical defence in the invasive red alga Gracilaria vermiculophylla. PLoS One 6, e29359CrossRefPubMedPubMedCentralGoogle Scholar
  54. Okino T, Yoshimura E, Hirota H, Fusetani N (1996) New antifouling kalihipyrans from the marine sponge Acanthella cavernosa. J Nat Prod 59:1081–1083CrossRefGoogle Scholar
  55. Okunade AL, Wiemer DF (1985) (-)-Loliolide, an ant-repellent compound from Xanthoxyllum setulosum. J Nat Prod 48:472–473CrossRefGoogle Scholar
  56. Othmani A, Bouzidi N, Viano Y, Alliche Z, Seridi H, Blache Y, El Hattab M, Briand J-F, Culioli G (2014) Anti-microfouling properties of compounds isolated from several Mediterranean Dictyota spp. J Appl Phycol 26:1573–1584Google Scholar
  57. Percot A, Yalçin A, Aysel V, Erdugan H, Dural B, Güven KC (2009) Loliolide in marine algae. Nat Prod Res 23:460–465CrossRefPubMedGoogle Scholar
  58. Persson F, Svensson R, Nylund GM, Fredriksson NJ, Pavia H, Hermansson M (2011) Ecological role of a seaweed secondary metabolite for a colonizing bacterial community. Biofouling 27:579–588CrossRefPubMedGoogle Scholar
  59. Piazza V, Roussis V, Garaventa F, Greco G, Smyrniotopoulos V, Vagias C, Faimali M (2011) Terpenes from the red alga Sphaerococcus coronopifolius inhibit the settlement of barnacles. Mar Biotechnol 13:764–772CrossRefPubMedGoogle Scholar
  60. Piazza V, Dragić I, Sepčić K, Faimali M, Garaventa F, Turk T, Berne S (2014) Antifouling activity of synthetic alkylpyridinium polymers using the barnacle model. Mar Drugs 12:1959–1976CrossRefPubMedPubMedCentralGoogle Scholar
  61. Puglisi MP, Sneed JM, Sharp KH, Ritson-Williams R, Paul VJ (2014) Marine chemical ecology in benthic environments. Nat Prod Rep 31:1510–1553CrossRefPubMedGoogle Scholar
  62. Qian P-Y, Xu Y, Fusetani N (2010) Natural products as antifouling compounds: recent progress and future perspectives. Biofouling 26:223–234CrossRefPubMedGoogle Scholar
  63. Qian P-Y, Chen L, Xu Y (2013) Mini-review: molecular mechanisms of antifouling compounds. Biofouling 29:381–400CrossRefPubMedGoogle Scholar
  64. Qiu J-W, Thiyagarajan V, Cheung S, Qian P-Y (2005) Toxic effects of copper on larval development of the barnacle Balanus amphitrite. Mar Pollut Bull 51:688–693CrossRefPubMedGoogle Scholar
  65. Qiu J-W, Hung OS, Qian P-Y (2008) An improved barnacle attachment inhibition assay. Biofouling 24:259–266CrossRefPubMedGoogle Scholar
  66. Rittschof D, Clare AS, Gerhart DJ, Mary SA, Bonaventura J (1992) Barnacle in vitro assays for biologically active substances: toxicity and settlement inhibition assays using mass cultured Balanus amphitrite amphitrite Darwin. Biofouling 6:115–122CrossRefGoogle Scholar
  67. Rohde S, Wahl M (2008) Antifeeding defense in baltic macroalgae: induction by direct grazing versus waterborne cues. J Phycol 44:85–90CrossRefPubMedGoogle Scholar
  68. Romano JA, Rittschof D, McClellan-Green PD, Holm ER (2010) Variation in toxicity of copper pyrithione among populations and families of the barnacle, Balanus amphitrite. Biofouling 26:341–347CrossRefPubMedGoogle Scholar
  69. Saha M, Wahl M (2013) Seasonal variation in the antifouling defence of the temperate brown alga Fucus vesiculosus. Biofouling 29:661–668CrossRefPubMedGoogle Scholar
  70. Saha M, Rempt M, Grosser K, Pohnert G, Weinberger F (2011) Surface-associated fucoxanthin mediates settlement of bacterial epiphytes on the rockweed Fucus vesiculosus. Biofouling 27:423–433CrossRefPubMedGoogle Scholar
  71. Saha M, Rempt M, Gebser B, Grueneberg J, Pohnert G, Weinberger F (2012) Dimethylsulphopropionate (DMSP) and proline from the surface of the brown alga Fucus vesiculosus inhibit bacterial attachment. Biofouling 28:593–604CrossRefPubMedGoogle Scholar
  72. Saha M, Rempt M, Stratil SB, Wahl M, Pohnert G, Weinberger F (2014) Defence chemistry modulation by light and temperature shifts and the resulting effects on associated epibacteria of Fucus vesiculosus. PLoS One 9, e105333CrossRefPubMedPubMedCentralGoogle Scholar
  73. Salta M, Wharton JA, Stoodley P, Dennington SP, Goodes LR, Werwinski S, Mart U, Wood RJK, Stokes KR (2010) Designing biomimetic antifouling surfaces. Phil Trans Roy Soc A 368:4729–4754CrossRefGoogle Scholar
  74. Scardino AJ, de Nys R (2010) Mini review: Biomimetic models and bioinspired surfaces for fouling control. Biofouling 27:73–86CrossRefGoogle Scholar
  75. Sera Y, Adachi K, Nishida F, Shizuri Y (1999) A new sesquiterpene as an antifouling substance from a Palauan marine sponge, Dysidea herbacea. J Nat Prod 62:395–396CrossRefPubMedGoogle Scholar
  76. Shaker KH, Müller M, Ghani MA, Dahse H-M, Seifert K (2010) Terpenes from the soft corals Litophyton arboreum and Sarcophyton ehrenbergi. Chem Biodivers 7:2007–2015CrossRefPubMedGoogle Scholar
  77. Sneed JM, Pohnert G (2011) The green alga Dicytosphaeria ocellata and its organic extracts alter natural bacterial biofilm communities. Biofouling 27:347–356CrossRefPubMedGoogle Scholar
  78. Sudatti DB, Rodrigues SV, Coutinho R, da Gama BAP, Salgado LT, Filho GMA, Pereira RC (2008) Transport and defensive role of elatol at the surface of the red seaweed Laurencia obtusa (Ceramiales, Rhodophyta). J Phycol 44:584–591CrossRefPubMedGoogle Scholar
  79. Taylor HF, Burden RS (1970) Identification of plant growth inhibitors produced by photolysis of violaxanthin. Phytochemistry 9:2217–2223CrossRefGoogle Scholar
  80. Thomas KV, Brooks S (2010) The environmental fate and effects of antifouling paint biocides. Biofouling 26:73–88CrossRefPubMedGoogle Scholar
  81. Tringali C, Piattelli M, Spatafora C (1995) Sesquiterpenes and geranylgeranylglycerol from the brown algae Taonia lacheana and Taonia atomaria f. ciliata : Their chemotaxonomic significance. Phytochemistry 40:827–831CrossRefGoogle Scholar
  82. Tziveleka L-A, Abatis D, Paulus K, Bauer R, Vagias C, Roussis V (2005) Marine polyprenylated hydroquinones, quinones, and chromenols with inhibitory effects on leukotriene formation. Chem Biodivers 2:901–909CrossRefPubMedGoogle Scholar
  83. Vairappan CS, Suzuki M, Ishii T, Okino T, Abe T, Masuda M (2008) Antibacterial activity of halogenated sesquiterpenes from Malaysian Laurencia spp. Phytochemistry 69:2490–2494CrossRefPubMedGoogle Scholar
  84. Vairappan C, Anangdan S, Tan K, Matsunaga S (2010) Role of secondary metabolites as defense chemicals against ice-ice disease bacteria in biofouler at carrageenophyte farms. J Appl Phycol 22:305–311CrossRefGoogle Scholar
  85. Viano Y, Bonhomme D, Camps M, Briand J-F, Ortalo-Magné A, Blache Y, Piovetti L, Culioli G (2009) Diterpenoids from the mediterranean brown alga Dictyota sp. evaluated as antifouling substances against a marine bacterial biofilm. J Nat Prod 72:1299–1304CrossRefPubMedGoogle Scholar
  86. Xu Y, He H, Schultz S, Liu X, Fusetani N, Xiong H, Xiao X, Qian P-Y (2010) Potent antifouling compounds produced by marine Streptomyces. Bioresource Technol 101:1331–1336CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Ahlem Othmani
    • 1
  • Robert Bunet
    • 2
  • Jean-Luc Bonnefont
    • 2
  • Jean-François Briand
    • 1
  • Gérald Culioli
    • 1
  1. 1.Université de ToulonMAPIEM EA 4323La Garde CedexFrance
  2. 2.Institut Océanographique Paul RicardIle des EmbiezSix-Fours-les-PlagesFrance

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