Journal of Applied Phycology

, Volume 28, Issue 5, pp 2865–2873 | Cite as

The yield and quality of multiple harvests of filamentous Ulva tepida

  • Christina Carl
  • Marie Magnusson
  • Nicholas A. Paul
  • Rocky de Nys


Species of the genus Ulva are used for human consumption due to their nutritional qualities and we assess a new filamentous species, Ulva tepida. A critical step is to quantify the yield and quality of biomass over multiple harvests to ensure consistency throughout the production cycle. To do this, ropes were seeded with U. tepida and harvested fortnightly over 6 weeks of outdoor cultivation with biomass yield and quality quantified for each harvest. This cycle was repeated a further two times. The yield of biomass was not significantly different between harvests (13.6–23.0 g dry weight (dw) m-1 rope), however, the final harvest was highly variable. Consequently, we recommend a production cycle of two harvests. The quality of biomass, as determined by the key biochemical parameters for these two sequential harvests, was consistent. Carbohydrates were the major component (45 % dw) and were primarily dietary fibre (27 % dw) consisting of insoluble (18 % dw) and soluble (9 % dw, equates to ulvan) fibre, with consistent values between harvests. Protein, as the sum of amino acids (17 % dw), was also consistent between harvests. Similarly, the content of ash (31 % dw) and lipids (3 % dw), as well as the composition of minerals and fatty acids was consistent. These results quantify, for the first time, no negative effects of multiple harvests on the yield and quality of biomass and support this technique to optimise productivity and quality.


Macroalgae Aquaculture Nutritional composition Ulvan Aonori 



This research is part of the MBD Energy Research and Development programme for the Integrated Production of Macroalgae. Furthermore, this research was supported by a Queensland Accelerate Fellowship of C. Carl from the Queensland Government in conjunction with MBD Energy Limited and Pacific Reef Fisheries as industry co-sponsors. We thank M. Martinez, A. Ricketts, Z. Loffler, K. Darlington and B. Boer for assistance with experiments. We also thank K-L. Dyer, M. Azmi Wahab and N. Neveux for the assistance with the biochemical analysis. The amino acid profiling was facilitated using infrastructure provided by the Australian Government through the National Collaborative Research Infrastructure Strategy (NCRIS).

Supplementary material

10811_2016_831_MOESM1_ESM.docx (418 kb)
ESM 1 (DOCX 418 kb)


  1. Adnan H, Prose H (1987) Culture of Eucheuma cottonii and Eucheuma spinosum in Indonesia. Hydrobiologia 151/152:355–358CrossRefGoogle Scholar
  2. Alves A, Pinho ED, Neves NM, Sousa RA, Reis RL (2012) Processing ulvan into 2D structures: cross-linked ulvan membranes as new biomaterials for drug delivery applications. Int J Pharm 426:76–81CrossRefPubMedGoogle Scholar
  3. Alves A, Sousa RA, Reis RL (2013a) A practical perspective on ulvan extracted from green algae. J Appl Phycol 25:407–424Google Scholar
  4. Alves A, Sousa RA, Reis RL (2013b) Processing of degradable ulvan 3D porous structures for biomedical applications. J Biomed Mater Res A 101A:998–1006Google Scholar
  5. Anderson MJ, Gorley R, Clarke K (2008) PERMANOVA + for PRIMER: Guide to software and statistical methods. Primer-E, PlymouthGoogle Scholar
  6. Angell AR, Mata L, de Nys R, Paul NA (2014) Variation in amino acid content and its relationship to nitrogen content and growth rate in Ulva ohnoi (Chlorophyta). J Phycol 50:216–226CrossRefPubMedGoogle Scholar
  7. Björnsäter BR, Wheeler PA (1990) Effect of nitrogen and phosphorous supply on growth and tissue composition of Ulva fenestrata and Enteromorpha intestinalis (Ulvaes, Chlorophyta). J Phycol 26:603–611CrossRefGoogle Scholar
  8. Bobin-Dubigeon C, Barr J (1997) Human colonic bacterial degradability of dietary fibres from sea-lettuce (Ulva sp). J Sci Food Agri 73:149–159CrossRefGoogle Scholar
  9. Bobin-Dubigeon C, Lahaye M, Guillon F, Barry J-L, Gallant DJ (1997) Factors limiting the biodegradation of Ulva sp cell-wall polysaccharides. J Sci Food Agric 75:341–351CrossRefGoogle Scholar
  10. Carl C, de Nys R, Paul NA (2014a) The seeding and cultivation of a tropical species of filamentous Ulva for algal biomass production. PLoS One 9(6):e98700Google Scholar
  11. Carl C, de Nys R, Lawton RJ, Paul NA (2014b) Methods for the induction of reproduction in a tropical species of filamentous Ulva. PLoS One 9(5):e97396Google Scholar
  12. Carl C, Lawton RJ, Paul NA, de Nys R (2016) Reproductive output and productivity of filamentous tropical Ulva over time. J Appl Phycol 28:429–438Google Scholar
  13. Champ M, Langkilde A-M, Brouns F, Kettlitz B, Collet Yle B (2003) Advances in dietary fibre characterisation. 1. Definition of dietary fibre, physiological relevance, health benefits and analytical aspects. Nutr Res Rev 16:71CrossRefPubMedGoogle Scholar
  14. Clarke K, Gorley R (2006) PRIMER v6: User manual/tutorial. Primer-E, PlymouthGoogle Scholar
  15. Cofrades S, López-López I, Solas MT, Bravo L, Jiménez-Colmenero F (2008) Influence of different types and proportions of added edible seaweeds on characteristics of low-salt gel/emulsion meat systems. Meat Sci 79:767–76CrossRefPubMedGoogle Scholar
  16. Cole AJ, de Nys R, Paul NA (2014) Removing constraints on the biomass production of freshwater macroalgae by manipulating water exchange to manage nutrient flux. PLoS One 9:e101284CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cordain L, Boyd Eaton S, Sebastion A, Mann N, Lindeberg S, Watkins BA, O’Keefe JH, Brand-Miller J (2005) Origins and evolution of the Western diet: health implications for the 21st Century. Am J Clin Nutr 81:341–354PubMedGoogle Scholar
  18. Cox S, Abu-Ghannam N (2013) Enhancement of the phytochemical and fibre content of beef patties with Himanthalia elongata seaweed. Int J Food Sci Technol 48:2239–2249Google Scholar
  19. de Souza Araújo DF, da Silva AMRB, de Andrade Lima LL, Vasconcelos MAS, Antrade SAC, Sarubbo LA (2014) The concentration of minerals and physicochemical contaminants in conventional and organic vegetables. Food Control 44:242–248CrossRefGoogle Scholar
  20. Du S, Neiman A, Batis C et al (2014) Understanding the patterns and trends of sodium intake, potassium intake, and sodium to potassium ratio and their effect on hypertension in China. Am J Clin Nutr 99:334–343CrossRefPubMedGoogle Scholar
  21. Elleuch M, Bedigian D, Roiseux O, Besbes S, Blecker C, Attia H (2011) Dietary fibre and fibre-rich by-products of food processing: characterisation, technological functionality and commercial applications: a review. Food Chem 124:411–421CrossRefGoogle Scholar
  22. Englyst HN, Hudson GJ (1996) The classification and measurement of dietary carbohydrates. Food Chem 57:15–21CrossRefGoogle Scholar
  23. Fuentes-Zaragoza E, Riquelme-Navarrete MJ, Sánchez-Zapata E, Pérez-Álvarez JA (2010) Resistant starch as functional ingredient: a review. Food Res Int 43:931–942CrossRefGoogle Scholar
  24. García-Casal MN, Ramírez J, Leets I, Pereira AC, Quiroga MF (2009) Antioxidant capacity, polyphenol content and iron bioavailability from algae (Ulva sp., Sargassum sp. and Porphyra sp.) in human subjects. Br J Nutr 101:79–85CrossRefPubMedGoogle Scholar
  25. 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 4:919–930CrossRefGoogle Scholar
  26. Grieshop CM, Fahey GC Jr (2001) Comparison of quality characteristics of soybeans from Brazil, China, and the United States. J Agric Food Chem 49:2669–2673CrossRefPubMedGoogle Scholar
  27. Gupta S, Abu-Ghannam N (2011) Recent developments in the application of seaweeds or seaweed extracts as a means for enhancing the safety and quality attributes of foods. Innov Food Sci Emerg Technol 12:600–609CrossRefGoogle Scholar
  28. Hafting JT, Critchley AT, Cornish ML, Hubley SA, Archibald AF (2012) On-land cultivation of functional seaweed products for human usage. J Appl Phycol 24:385–392CrossRefGoogle Scholar
  29. Hanif R, Iqbal Z, Iqbal M, Hanif S, Rasheed M (2006) Use of vegetables as nutritional food: role in human health. J Agric Biol Sci 1:18–22Google Scholar
  30. Hernández-Garibay E, Zertuche-González JA, Pacheco-Ruíz I (2011) Isolation and chemical characterization of algal polysaccharides from the green seaweed Ulva clathrata (Roth) C. Agardh. J Appl Phycol 23:537–542CrossRefGoogle Scholar
  31. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  32. Kawashima Y, Akasaki T, Matsumoto Y, Yamazaki Y, Shimada S (2013) Species identification of imported and Japanese commercial green algal products based on phylogenetic analyses using the nrITS2 and 5S rDNA spacer regions. Fish Sci 79:521–529CrossRefGoogle Scholar
  33. Lahaye M (1991) Marine algae as sources of fibres: determination of soluble and insoluble dietary fibre contents in some “sea vegetables.”. J Sci Food Agri 54:587–594CrossRefGoogle Scholar
  34. Lahaye M, Jegou D (1993) Chemical and physical-chemical characteristics of dietary fibres from Ulva lactuta (L.) and Enteromorpha compressa (L.) Grev. J Appl Phycol 5:195–200CrossRefGoogle Scholar
  35. Lahaye M, Robic A (2007) Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1765–74CrossRefPubMedGoogle Scholar
  36. Lahaye M, Gomez-Pinchetti J-L, del Rio MJ, Garcia-Reina G (1995) Natural decoloration, composition and increase in dietary fibre content of an edible marine algae, Ulva rigida (Chlorophyta), grown under different nitrogen conditions. J Sci Food Agri 68:99–104CrossRefGoogle Scholar
  37. Lawton RJ, Mata L, de Nys R, Paul NA (2013) Algal bioremediation of waste waters from land-based aquaculture using Ulva: selecting target species and strains. PLoS One 8(10):e77344CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lobban CS, Harrison PJ (1997) Seaweed ecology and physiology. Cambridge University Press, CambridgeGoogle Scholar
  39. Mabeau S, Fleurence J (1993) Seaweed in food products: biochemical and nutritional aspects. Trends Food Sci Technol 4:103–107CrossRefGoogle Scholar
  40. MacArtain P, Gill CIR, Brooks M et al (2007) Nutritional value of edible seaweeds. Nutr Rev 656:535–543CrossRefGoogle Scholar
  41. Mahesh DL, Deosthale YG, Rao BSN (1992) A sensitive kinetic assay for the determination of iodine in foodstuffs. Food Chem 43:51–56CrossRefGoogle Scholar
  42. Marsham S, Scott GW, Tobin ML (2007) Comparison of nutritive chemistry of a range of temperate seaweeds. Food Chem 100:1331–1336CrossRefGoogle Scholar
  43. Masakiyo Y, Shimada S (2014) Species diversity of the genus Ulva (Ulvophyceae, Chloropytha) in Japanese waters, with special reference to Ulva tepida Masakiyo et S. Shimada sp. nov. Bull Natl Mus Nat Sci Ser B 40:1–13Google Scholar
  44. Mata L, Magnusson M, Paul NA, de Nys R (2016) The intensive land-based production of the green seaweeds Derbesia tenuissima and Ulva ohnoi: biomass and bioproducts. J Appl Phycol 28:365–375Google Scholar
  45. McDermid KJ, Stuercke B (2003) Nutritional composition of edible Hawaiian seaweeds. J Appl Phycol 15:513–524CrossRefGoogle Scholar
  46. McHugh DJ (2003) A guide to the seaweed industry, FAO Fisheries Technical Paper No. 441Google Scholar
  47. Melnik G, Brooks MJ, Torosian MH (1995) Total Parenteral Nutrition Solutions. In: Torosian MH (ed) Nurtition for the hospitalized patient: basic science and principles of practice. CRC Press, New York, USA, pp 271–292Google Scholar
  48. Navarro-Angulo L, Robledo D (1999) Effects of nitrogen source, N:P ratio and N-pulse concentration and frequency on the growth of Gracilaria cornea (Gracilariales, Rhodophyta) in culture. Hydrobiologia 398/399:315–320CrossRefGoogle Scholar
  49. Neveux N, Yuen AKL, Jazrawi C, Magnussen M, Haynes BS, Masters AF, Montoya A, Paul NA, Maschmeyer T, de Nys R (2014) Pre- and post-harvest treatment of macroalgae to improve the quality of feedstock for hydrothermal liquefaction. Algal Res 6:22–31CrossRefGoogle Scholar
  50. Neveux N, Magnusson M, Maschmeyer T, de Nys R, Paul NA (2015) Comparing the potential production and value of high-energy liquid fuels and protein from marine and freshwater macroalgae. GCB Bioenergy 7:673–689CrossRefGoogle Scholar
  51. Ohno M (1993) Cultivation of the green algae, Monostroma and Enteromorpha “Aonori.”. In: Ohno M, Critchley AT (eds) Seaweed cultivation and marine ranching. Japan International Cooperation Agency, Jokosuka, pp 7–16Google Scholar
  52. Ohno M (2006) Recent developments in the seaweed cultivation and industry in Japan. In: Advances in seaweed cultivation and utilisation in Asia: proceedings of a workshop held in conjunction with the 7th Asian Fisheries Forum, Penang. University of Malaya, Kuala Lumpur, pp 1–20Google Scholar
  53. Ohno M, Mairh O, Chauhan V, Tewari A, Oza RM, Joshi HV, Pandfey RS, Rao PS (1981) Mass cultivation of green alga Enteromorpha on the coast of Okha, India. Rep Usa Mar Biol Inst 3:51–59Google Scholar
  54. Ortiz J, Romero N, Robert P, Araya J, Lopez-Hernández J, Bozzo C, Navarrete E, Osorio A, Rios A (2006) Dietary fiber, amino acid, fatty acid and tocopherol contents of the edible seaweeds Ulva lactuca and Durvillaea antarctica. Food Chem 99:98–104CrossRefGoogle Scholar
  55. Pan A, Chen M, Chowdhury R, Wu JH, Sun Q, Campos H, Mozaffarian D, Hu FB (2012) α-Linolenic acid and risk of cardiovascular disease: a systematic review and meta-analysis. Am J Clin Nutr 96:1262–1273CrossRefPubMedPubMedCentralGoogle Scholar
  56. Pandey RS, Ohno M (1985) An ecological study of cultivated Enteromorpha. Rep Usa Mar Biol Inst 7:21–31Google Scholar
  57. Phillips JA, Lawton RJ, de Nys R, Paul NA, Carl C (2016) Ulva sapora sp. nov., a new abundant tubular species of Ulva (Ulvales) from the tropical Pacific Ocean. Phycologia 55:55–64CrossRefGoogle Scholar
  58. Roberts DA, de Nys R, Paul NA (2013) The effect of CO2 on algal growth in industrial waste water for bioenergy and bioremediation applications. PLoS One 8(11):e81631CrossRefPubMedPubMedCentralGoogle Scholar
  59. Ross AB, Jones JM, Kubacki ML, Bridgeman T (2008) Classification of macroalgae as fuel and its thermochemical behaviour. Bioresour Technol 99:6494–504CrossRefPubMedGoogle Scholar
  60. Schmitz G, Ecker J (2008) The opposing effects on n-3 and n-6 fatty acids. Prog Lipid Res 47:147–155CrossRefPubMedGoogle Scholar
  61. Shimada S, Yokoyama N, Arai S, Hiraoka M (2008) Phylogeography of the genus Ulva (Ulvophyceae, Chlorophyta), with special reference to the Japanese freshwater and brackish taxa. J Appl Phycol 20:979–989CrossRefGoogle Scholar
  62. Shuuluka D, Bolton JJ, Anderson RJ (2013) Protein content, amino acid composition and nitrogen-to-protein conversion factors of Ulva rigida and Ulva capensis from natural populations and Ulva lactuca from an aquaculture system, in South Africa. J Appl Phycol 25:677–685CrossRefGoogle Scholar
  63. Simopoulos AP (2002) The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother 56:365–379CrossRefPubMedGoogle Scholar
  64. Sterner RW, Elser JJ (2002) Ecological stoichiometry. Princeton University Press, PrincetonGoogle Scholar
  65. Suter PM, Sierro C, Vetter W (2002) Nutritional factors in the control of blood pressure and hypertension. Nutr Clin Care 5:9–19CrossRefPubMedGoogle Scholar
  66. Suttle NF (2010) Mineral nutrition of livestock, 4th edn. CABI, WallingfordCrossRefGoogle Scholar
  67. U.S. Department of Agriculture and U.S. Department of Health and Human Services (2010) Dietary guidelines for Americans 2010, 7th edition, WashingtonGoogle Scholar
  68. van der Wal H, Sperber BLHM, Houweling-Tan B, Bakker RRC, Brandenburg W, López-Contreras AM (2013) Production of acetone, butanol, and ethanol from biomass of the green seaweed Ulva lactuca. Bioresour Technol 128:431–437CrossRefPubMedGoogle Scholar
  69. Wang L, Wang X, Wu H, Liu R (2014) Overview on biological activities and molecular characteristics of sulfated polysaccharides from marine green algae in recent years. Mar Drugs 12:4984–5020CrossRefPubMedPubMedCentralGoogle Scholar
  70. Wong KH, Cheung PCK (2000) Nutritional evaluation of some subtropical red and green seaweeds. Part I - proximate composition, amino acid profiles and some physico-chemical properties. Food Chem 71:475–482Google Scholar
  71. Yaich H, Garna H, Besbes S, Paquot M, Blecker C, Attia H (2013) Effect of extraction conditions on the yield and purity of ulvan extracted from Ulva lactuca. Food Hydrocoll 31:375–382CrossRefGoogle Scholar
  72. Yaich H, Garna H, Bchir B, Besbes S, Paquot M, Richel A, Blecker C, Attia H (2015) Chemical composition and functional properties of dietary fibre extracted by Englyst and Prosky methods from the alga Ulva lactuca collected in Tunisia. Algal Res 9:65–73CrossRefGoogle Scholar
  73. Zhuang Y, Guo J, Chen L, Li D, Liu J, Ye N (2012) Microwave-assisted direct liquefaction of Ulva prolifera for bio-oil production by acid catalysis. Bioresour Technol 116:133–139CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Christina Carl
    • 1
  • Marie Magnusson
    • 1
  • Nicholas A. Paul
    • 1
  • Rocky de Nys
    • 1
  1. 1.MACRO – the Centre for Macroalgal Resources and Biotechnology, College of Marine and Environmental SciencesJames Cook UniversityTownsvilleAustralia

Personalised recommendations