Caulerpa consumption, nutritional value and farming in the Indo-Pacific region

Journal of Applied Phycology

Volumn 29, Issue 5, 2017, Pages 2249-2266

  de Gaillande, Clara ^a   Payri, Claude ^b   Remoissenet, Georges ^b   Zubia, Mayalen ^a  

^a UNIVERSITÉ DE LA POLYNÉSIE FRANÇAISE   (French Polynesia)

^b IRD Nouméa ^*  (French Polynesia)

Author keywords

Caulerpa; Human food; Nutrition; Seaweed farming

Indexed keywords

EID: 84980007962     PISSN: 09218971     EISSN: 15735176     Source Type: Journal    
DOI: 10.1007/s10811-016-0912-6     Document Type: Conference Paper

References (113)

1. Abbott IA (1991) Polynesian uses of seaweed. In: Cox PA, Banack SA (eds) Islands, plants and Polynesians: an introduction to Polynesian ethnobotany, Dioscorides Press, Portland, Oregon, pp135–145.
2. Amade P, Lemee R (1998) Chemical defense of the Mediterranean alga Caulerpa taxifolia: variations in caulerpenyne production. Aquat Toxicol 43:287–300
3. Aneiros A, Garateix A (2004) Bioactive peptides from marine sources: pharmacological properties and isolation procedures. J Chromatogr B 803:41–53
4. Barbier P, Guise S, Huitorel P, Amade P, Pesando D, Briand C, Peyrot V (2001) Caulerpenyne from Caulerpa taxifolia has an antiproliferative activity on tumor cell line SK-N-SH and modifies the microtubule network. Life Sci 70:415–429
5. Bast F (2013) Agronomy and cultivation methods for edible seaweeds. Int J Agri Food Sci Tech 4:661–666
6. Bell JD, Andrew NL, Batty MJ, Chapman LB, Dambacher JM, Dawson B, Ganachaud AS, Gehrke PC, Hampton J, Hobday AJ, Hoegh-Guldberg O, Johnson JE, Kinch JP, Le Borgne R, Lehodey P, Lough JM, Pickering TD, Pratchett MS, Vunisea A, Waycott M (2011). Adapting tropical Pacific fisheries and aquaculture to climate change: Management measures, policies and investments. In: Bell JD, Johnson JE and Hobday AJ (eds) Vulnerability of tropical Pacific fisheries and aquaculture to climate change. Secretariat of the Pacific Community, Noumea, New Caledonia, pp 803–876
7. Belton GS, van Prud’homme Reine WF, Huisman JM, Draisma SGA, Gurgel CFD (2014) Resolving phenotypic plasticity and species designation in the morphologically challenging Caulerpa racemosa-peltata complex (Chlorophyta, Caulerpaceae). J Phycol 50:32–54
8. Bocanegra A, Bastida S, Benedi J, Rodenas S, Sanchez-Muniz FJ (2009) Review—characteristics and nutritional and cardiovascular-health properties of seaweeds. J Med Food 12:236–258
9. Bodiguel C (1996) L’algoculture dans le monde et ses contraintes. Annales de Géographie 591:480–497
10. Burkholder PR, Burkholder LM, Almodovar LR (1971) Nutritive constituents of some Caribbean marine algae. Bot Mar 14:132–135
11. Calvert HE, Dawes CJ, Borowitzka MA (1976) Phylogenetic relationships of Caulerpa (Chlorophyta) based on comparative chloroplast ultrastructure. J Phycol 12:149–162
12. Carneiro JG, Rodriguez JAG, Teles FB, Belfort A, Cavalcante D, Benevides NMB (2014) Analysis of some chemical nutrients in four Brazilian tropical seaweeds. Acta Scientiarum Biol Sci, 36:137–145
13. Cavas L, Yurdakoc K (2005) A comparative study: assessment of the antioxidant system in the invasive green alga Caulerpa racemosa and some macrophytes from the Mediterranean. J Exp Mar Biol Ecol 321:35–41
14. Cavas L, Baskin Y, Yurdakoc K, Olgun N (2006) Antiproliferative and newly attributed apoptotic activities from an invasive marine algae: Caulerpa racemosa var. cylindracea. J Exp Mar Biol Ecol 339:111–119
15. Chamberlain A, Pickering T (1998) Post harvest handling of Caulerpa racemosa for artisanal and export fisheries in Fiji. In: Fisheries and marine resources. Marine Studies Programme Technical Report 3:90–102
16. Chopin T, Buschmann AH, Halling C, Troell M, Kautsky N, Neori A, Kraemer GP, Zertuche-Gonzalez JA, Yarish C, Neefus C (2001) Integrating seaweeds into marine aquaculture systems: a key towards sustainability. J Phycol 37:975–986
17. Chopin T (2012) Seaweed aquaculture provides diversified products, key ecosystem functions. Part II recent evolution of seaweed industry. Global Aquacult Adv 14:24–27
18. Conte E, Payri C (2002) La consommation des algues en Polynésie française: premiers résultats d’une enquête. Le Journal de la Société des Océanistes 114–115:165–172
19. Conte E, Payri C (2006) Present day consumption of edible algae in French Polynesia: a study of the survival of pre-European practices. J Polynesian Soc 115:77–93
20. Consolacion R, Ebajo J, Lazaro-Llanos N, Brkljaca R, Urban S (2015) Secondary metabolites from Caulerpa racemosa. Der Pharmacia Lettre 7(10):122–125
21. Costa MSSP, Costa LS, Cordeiro SL, Almeida-Lima J, Dantas-Santos N, Magalhães KD, Sabry DA, Albuquerque IRL, Pereira MR, Leite EL, Rocha HAO (2012) Evaluating the possible anticoagulant and antioxidant effects of sulfated polysaccharides from the tropical green alga Caulerpa cupressoides var. flabellata. J Appl Phycol 24:1159–1167
22. Da Conceição Rivanor RL, Chaves HV, Do Val DR, de Freitas AR, Lemos JC, Rodrigues JAG, Benevides NMB (2014) A lectin from the green seaweed Caulerpa cupressoides reduces mechanical hyper-nociception and inflammation in the rat temporomandibular joint during zymosan-induced arthritis. Int Immunopharmacol 21:34–43
23. Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fiber in edible seaweed products. Food Chem 103:891–899
24. De Haro LM, Treffor J, Jouglard J, Perringue C (1993) Trois cas d’intoxication de type ciguateresque apres ingestion de Sparidae de Mediterranée. Ichthyophysiol Acta 16:133–146
25. de Souza E, Pereira de Lira D, Cavalcanti de Queiroz A, José Costa da Silva D, Bezerra de Aquino A, Czmpessato Mella EA, Prates Lorenzo V, de Miranda GEC, de Araujo-Junior JX, de Oliveira Chaves MC, Barbossa-Filho JM, de Athayde-Filho PF, de Oliveira Santos BV, Alexandre-Moreira MS (2009) The antinociceptive and anti-inflammatory activities of caulerpin, a bisindole alkaloid isolated from seaweeds of the genus Caulerpa. Mar Drugs 7:689–704
26. Dumay O, Pergent G, Pergent-Martini C, Amade F (2002) Variations in caulerpenyne contents in Caulerpa taxifolia and Caulerpa racemosa. J Chem Ecol 28:343–352
27. FAO (2014) The State of World Fisheries and Aquaculture. FAO, Rome
28. Famá P, Wysor B, Kooistra WHCF, Zuccarello GC (2002) Molecular phylogeny of the genus Caulerpa (Caulerpales, Chlorophyta) inferred from chloroplast tufA gene. J Phycol 38:1040–1050
29. Fleurence J (1999) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Technol 10:25–28
30. Fleurence J, Morançais M, Decottignies P, Turpin V, Munier M, Garcia-Bueno N, Jaouen P (2012) What are the prospects for using seaweed in human nutrition and for marine animals raised through aquaculture? Trends Food Sci Technol 27:57–61
31. Flores SR, Dobbs J, Dunn MA (2015) Mineral nutrient content and iron bioavailability in common and Hawaiian seaweeds assessed by an in vitro digestion/Caco-2 cell model. J Food Compos Anal 43:185–193
32. Ghosh P, Adhikari U, Ghossal PK, Pujol CA, Carlucci MJ, Damonte EB, Ray B (2004) In vitro anti-herpetic activity of sulfated polysaccharide fractions from Caulerpa racemosa. Phytochem 65:3151–3157
33. Gosch BJ, Magnusson M, Paul NA, de Nys R (2012) Total lipid and fatty acid composition of seaweeds for the selection of species for oil-based biofuel and bioproducts. GCB Bioenergy 4:919–930
34. Guerriero A, Meinesz A, D’Ambrosia M, Pietra F (1992) Isolation of toxic and potentially toxic sesqui- and monoterpenes from the tropical green seaweed Caulerpa taxifolia which has invaded the region of Cap Martin and Monaco. Helv Chim Acta 75:689–695
35. Guiry MD, Guiry GM (2016) AlgaeBase. Worldwide electronic publication, National University of Ireland, Galway. http://www.algaebase.org. Accessed 18 April 2016.
36. Hayakawa Y, Hayashi T, Lee JB, Srisomporn P, Maeda M, Ozawa T, Sakuragawa N (2000) Inhibition of thrombin by sulfated polysaccharides isolated from green algae. Biochim Biophys Acta 1543:86–94
37. Hong DD, Hien HM, Son PN (2007) Seaweeds from Vietnam used for functional food, medicine and biofertilizer. J Appl Phycol 19:817–826
38. Horstmann U (1983) Cultivation of the green alga, Caulerpa racemosa, in tropical waters and some aspects of its physiological ecology. Aquaculture 32:361–371
39. Jakobsdottir G, Nyman M, Fak F (2014) Designing future prebiotic fiber to target metabolic syndrome. Nutrition 30:497–502
40. Ji H, Shao H, Zhang C, Hong P, Xiong H (2008) Separation of the polysaccharides in Caulerpa racemosa and their chemical composition and antitumor activity. J Appl Polym Sci 110:1435–1440
41. Joint WHO (2007) Protein and amino acid requirements in human nutrition. World Organ Tech Rep Ser 935
42. Jung V, Thibaut T, Meinesz A, Pohnert G (2002) Comparison of the wound-activated transformation of caulerpenyne by invasive and noninvasive Caulerpa species of the Mediterranean. J Chem Ecol 28:2091–2105
43. Kawaroe M, Prartono T, Kusuma AH (2013) Effect of acid concentration on hydrolysis efficiency on Caulerpa racemosa, Sargassum crassifolium and Gracilaria salicornia. Int J Envir Bioenergy 8:127–134
44. Khan G (1990) Status of production and utilization of seaweeds Bangladesh. Part II: country status reports. Report of the Regional Workshop on the Culture & Utilization of Seaweeds, FAO, Cebu City, Philippines, pp 27–31
45. Khotimchenko SV (1995) Fatty acid composition of green algae of the genus Caulerpa. Bot Mar:509–512
46. Kohen R, Nyska A (2002) Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and method for their quantification. Toxicol Pathol 30:620–650
47. Kornprobst JM (2005) Substances naturelles d’origine marine: Chimiodiversité, Pharmacodiversité, Biotechnologies, Tecan Doc, Lavoisier, Paris
48. Kumar M, Kumari P, Trivedi N, Shukla MK, Gupta V, Reddy CRK, Jha R (2011) Minerals, PUFAs and antioxidant properties of some tropical seaweeds from Saurashtra coast of India. J Appl Phycol 23:797–810
49. Kumari P, Bijo AJ, Mantri VA, Reddy CRK, Jha B (2013) Fatty acid profiling of tropical marine macroalgae: an analysis from chemotaxonomic and nutritional perspectives. Phytochem 86:44–56
50. Kumari P, Kumar M, Gupta V, Reddy CRK, Jha B (2010) Tropical marine macroalgae as potential sources of nutritionally important PUFAs. Food Chem 120:749–757
51. Lam C, Harder T (2007) Marine macroalgae affect abundance and community richness of bacterioplankton in close proximity. J Phycol 43:874–881
52. Lemée R, Pesando D, Durand-Clément M, Dubreuil A, Meinesz A, Guerriero A, Pietra F (1993) Preliminary survey of toxicity of the green alga Caulerpa taxifolia introduced into the Mediterranean. J Appl Phycol 5:485–493
53. Li Z, Wang B, Zhang Q, Qu Y, Xu H, Li G (2012) Preparation and antioxidant property of extract and semi-purified fractions of Caulerpa racemosa. J Appl Phycol 24:1527–1536
54. Lin HC, Chou ST, Chuang MY, Liao TY, Tsai WS, Chiu TH (2012) The effects of Caulerpa microphysa enzyme-digested extracts on ACE-inhibitory activity and in vitro anti-tumour properties. Food Chem 134:2235–2241
55. Liu AH, Liu DQ, Liang TJ, XQ Y, Feng MT, Yao LG, Mao SC (2013) Caulerprenylols a and B, two rare antifungal prenylated para-xylenes from the green alga Caulerpa racemosa. Bioorg Med Chem Lett 23:2491–2494
56. Liu H, Wang F, Wang Q, Dong S, Tian X (2016) A comparative study of the nutrient uptake and growth capacities of seaweeds Caulerpa lentillifera and Gracilaria lichenoides. J Appl Phycol. doi:10.1007/s10811-016-0858-8
57. MacArtain P, Gill CI, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65:535–543
58. Maeda R, Ida T, Ihara H, Sakamoto T (2012) Immunostimulatory activity of polysaccharides isolated from Caulerpa lentillifera on macrophage cells. Biosci Biotechnol Biochem 76:501–505
59. Marquez GPB, Santianez WJE, Trono GC, Montano MNE, Araki H, Takeuchi H, Hasegawa T (2014) Seaweed biomass of the Philippines: sustainable feedstock for biogas production. Renew Sust Energ Rev 38:1056–1068
60. Mary A, Mary V, Lorella A, Matias JR (2009) Rediscovery of naturally occurring seagrape Caulerpa lentillifera from the Gulf of Mannar and its mariculture. Curr Sci 97:1418–1420
61. Mata L, Wright E, Owens L, Paul N, de Nys R (2013) Water-soluble natural products from seaweed have limited potential in controlling bacterial pathogens in fish aquaculture. J Appl Phycol 25:1963–1973
62. Matanjun P, Mohamed S, Mustapha NM, Muhammad K, Ming CH (2008) Antioxidant activities and phenolics content of eight species of seaweeds from north Borneo. J Appl Phycol 20:367–373
63. Matanjun P, Mohamed S, Mustapha NM, Muhammad K (2009) Nutrient content of tropical edible seaweeds, Eucheuma cottonii Caulerpa lentillifera and Sargassum polycystum. J Appl Phycol 21:75–80
64. Mayakrishnan V, Kannappan P, Abdullah N, Ahmed ABA (2013) Cardioprotective activity of polysaccharides derived from marine algae: an overview. Trends Food Sci Technol 30:98–104
65. McDermid KJ, Stuercke B (2003) Nutritional composition of edible Hawaiian seaweeds. J Appl Phycol 15:513–524
66. McHugh DJ (2003) A guide to the seaweed industry. FAO, Rome
67. Meyer KD, Paul VJ (1992) Intraplant variation in secondary metabolite concentration in three species of Caulerpa (Chlorophyta:Caulerpales) and its effects on herbivorous fishes. Mar Ecol Prog Ser 82:249–257
68. Mintardjo K (1990) Status of production and utilization of seaweeds Indonesia. Part II: country status reports. Report of the Regional Workshop on the Culture & Utilization of Seaweeds, FAO, Cebu City, Philippines, pp 27–31
69. Mišurcová L, Machů L, Orsavová J (2011) Seaweed minerals as nutraceuticals. Adv Food Nutr Res 64:371–390
70. Mišurcová L, Buňka F, Ambrožová JV, Machů L, Samek D, Kráčmar S (2014) Amino acid composition of algal products and its contribution to RDI. Food Chem 151:120–125
71. Mohamed S, Hashim SN, Rahman A (2012) Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends Food Sci Technol 23:83–96
72. Morris C, Bala S, South GR, Lako J, Lober M, Simos T (2014) Supply chain and marketing of sea grapes, Caulerpa racemosa (Forsskål) J. Agardh (Chlorophyta: Caulerpaceae) in Fiji, Samoa and Tonga. J Appl Phycol 26:783–789
73. Mozzachiodi R, Scuri R, Roberto M, Brunelli M (2001) Caulerpenyne, a toxin from the seaweed Caulerpa taxifolia, depresses after hyperpolarization in invertebrate neurons. Neuroscience 107:519–526
74. Nagappan T, Vairappan CS (2014) Nutritional and bioactive properties of three edible species of green algae, genus Caulerpa (Caulerpaceae). J Appl Phycol 26:1019–1027
75. Newton IS (1996) Long chain fatty acids in health and nutrition. J Food Lipids 3:233–249
76. Ngo DH, Vo TS, Ngo DN, Wijesekara I, Kim SK (2012) Biological activities and potential health benefits of bioactive peptides derived from marine organisms. Int J Biol Macromol 51:378–383
77. Nguyen VT, Ueng JP, Tsai GJ (2011) Proximate composition, total phenolic content, and antioxidant activity of seagrape (Caulerpa lentillifera). J Food Sci 76:950–958
78. Nieminen V, Laakso P, Kuusisto P, Niemelä J, Laitinen K (2016) Plant stanol content remains stable during storage of cholesterol-lowering functional foods. Food Chem 196:1325–1330
79. Ohno M (1990) Status of production and utilization of seaweeds Japan. Part II: country status reports. Report of the Regional Workshop on the Culture & Utilization of Seaweeds, FAO, Cebu City, Philippines, pp 27–31
80. Ostraff M (2006) Limu: edible seaweed in Tonga, an ethnobotanical study. J Ethnobiol 26:208–227
81. Pang SJ, Xiao T, Bao Y (2006) Dynamic changes of total bacteria and vibrio in an integrated seaweed–abalone culture system. Aquaculture 252:289–297
82. Paul NA, Neveux N, Magnusson M, De Nys R (2014) Comparative production and nutritional value of “sea grapes”—the tropical green seaweeds Caulerpa lentillifera and Caulerpa racemosa. J Appl Phycol 26:1833–1844
83. Paul VJ, Arthur KE, Ritson-Williams R, Ross C, Sharp K (2007) Chemical defenses: from compounds to communities. Biol Bull 231:226–251
84. Paul VJ, Fenical W (1986) Chemical defense in tropical green algae, order Caulerpales. Mar Ecol Prog Ser 34:157–169
85. Pesando D, Lemee R, Ferrua C, Amade P, Girard JP (1996) Effects of caulerpenyne, the major toxin from Caulerpa taxifolia on mechanisms related to sea urchin egg cleavage. Aquat Toxicol 35:139–155
86. Ponia B (2010) A review of aquaculture in the Pacific Islands 1998–2007: tracking a decade of progress through official and provisional statistics, Noumea, New-Caledonia, Secretariat of Pacific Community.
87. Radulovitch R, Umanzor S, Cabrera R, Mata R (2015) Tropical seaweeds for human food, their cultivation and its effect on biodiversity enrichment. Aquaculture 436:40–46
88. Ratana-arpon P, Chirapart A (2006) Nutritional evaluation of tropical green seaweeds Caulerpa lentillifera and Ulva reticulata. Kasetsart. J Nat Sci 40:75–83
89. Renaud SM, Luong-Van JT (2006) Seasonal variation in the chemical composition of tropical Australian marine macroalgae. J Appl Phycol 18:381–387
90. Ribeiro NA, Abreu TM, Chaves HV, Bezerra MM, Monteiro HSA, Jorge RJB, Benevides NMB (2014) Sulfated polysaccharides isolated from the green seaweed Caulerpa racemosa plays antinociceptive and anti-inflammatory activities in a way dependent on HO-1 pathway activation. Inflamm Res 63:569–580
91. Rupérez P (2002) Mineral content of edible marine seaweeds. Food Chem 79:23–26
92. Robledo D, Freile-Pelegrin Y (1997) Chemical and mineral composition of six potentially edible seaweed species of Yucatan. Bot Mar 40:301–306
93. Robledo D, Freile-Pelegrin Y 2005 Seasonal variation in photosynthesis and biochemical composition of Caulerpa spp. (Bryopsidales, Chlorophyta) from the Gulf of Mexico. Phycologia 44:312–319
94. Rodrigues JAG, Vanderlei EdSO, Silva LMCM, de Araújo IWF, de Queiroz INL, de Paula GA, Abreu TM, Ribeiro NA, Bezerra MM, Chaves HV, Lima V, Jorge RJB, Monteiro HSA, Leite EL, Benevides NMB (2012) Antinociceptive and anti-inflammatory activities of a sulfated polysaccharide isolated from the green seaweed Caulerpa cupressoides. Pharm Rep 64:282–292
95. Santoso J, Gunji S, Yoshie-Stark Y, Suzuki T (2006) Mineral contents of Indonesia seaweeds and mineral solubility affected by basic cooking. Food Sci Technol Res 12:59–66
96. Santoso J, Yoshie-Stark Y, Suzuki T (2004) Antioxidant activity of methanol extracts from Indonesian seaweeds in an oil emulsion model. Fish Sci 70:183–188
97. Sauvage T, Payri C, Draisma SGA, van Prud’homme Reine W, Verbruggen H, Belton GS, Frederico DG, Gabriel D, Sherwood AR, Fredericq S (2013) Molecular diversity of the Caulerpa racemosa-Caulerpa peltata complex (Caulerpaceae, Bryopsidales) in New Caledonia, with new Australasian records for C. racemosa var. cylindracea. Phycologia 52:6–13
98. Schmitt TM, Hay ME, Linquist N (1995) Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology 76:107–123
99. Shameel M (1990) Phycochemical studies on fatty acids from certain seaweeds. Bot Mar 33:429–432
100. Shameel M, Khan R (1991) Fatty acid composition of nine green seaweeds. Bot Mar 34:501–504
101. South GR (1993) Edible seaweeds of Fiji: an ethnobotanical study. Bot Mar 36:335–349
102. South GR, Morris C, Bala S, Lober M (2012) Value adding and supply chain development for fisheries and aquaculture products in Fiji, Samoa and Tonga: scoping study for Caulerpa (Seagrapes). Suva, Fiji: Institute of Marine Resources, School of Marine Studies, IMR Technical Report
103. Special Food Vietnam (2014) http://specialfoodvietnam.com/news/seaweed-farming-sea-grape-caulerpa-lentillifera-sea-grape/201
104. Tanduyan SN, Gonzaga RB, Bensig VD (2013) Off bottom culture of Caulerpa lentillifera in three different water levels in the marine waters of San Francisco, Cebu, Philippines. J Coral Reef Stud 155:123–132
105. Titlyanov EA, Titlyanova TV (2010) Seaweed cultivation: methods and problems. Russ J Mar Biol 36:227–242
106. Trono GC(1988) Manual on seaweed culture 2. Pond culture of Caulerpa and 3. Pond culture of Gracilaria. ASEAN/UNPD/DF/FAO Regional Small-Scale Coastal Fisheries Development Project, Manila, Philippines. ASEAN/SF/88/Manual No. 3
107. Trono GC (1990) Status of production and utilization of seaweeds in the Philippines. Part II: country status reports. Report of the Regional Workshop on the Culture & Utilization of Seaweeds, FAO, Cebu City, Philippines, pp 27–31
108. Van Ginneken VJ, Helsper JP, de Visser W, van Keulen H, Brandenburg WA (2011) Polyunsaturated fatty acids in various macroalgal species from North Atlantic and tropical seas. Lipids Health Dis 10(1):104. Doi:10.1186/1476-511x-10-104
109. Watanabe F, Yabuta Y, Bito T, Teng F (2013) Vitamin B12-containing plant food sources for vegetarians. Nutrition 6:1861–1873
110. Wikfors GH, Ohno M (2001) Impact of algal research in aquaculture. J Phycol 37:968–974
111. Yangthong M, Hutadilok-Towatana N, Phromkunthong W (2009) Antioxidant activities of four edible seaweeds from the southern coast of Thailand. Plant Foods Hum Nutr 64:218–223
112. Zafar M (2005) Seaweed culture in Bangladesh holds promise. In: Infofish International 1/2005, January/February, pp. 8–10
113. Zubia M, Robledo D, Freile-Pelegrin Y (2007) Antioxidant activities in tropical marine macroalgae from the Yucatan Peninsula, Mexico. J Appl Phycol 19:449–458