Advertisement

Journal of Applied Phycology

, Volume 29, Issue 5, pp 2417–2426 | Cite as

Nutritional value of the kelps Alaria esculenta and Saccharina latissima and effects of short-term storage on biomass quality

  • Pierrick Stévant
  • Hélène Marfaing
  • Turid Rustad
  • Ingrid Sandbakken
  • Joël Fleurence
  • Annelise Chapman
22ND INTERNATIONAL SEAWEED SYMPOSIUM, COPENHAGEN

Abstract

Storage of macroalgae in seawater, prior to further processing, is a standard initial pre-treatment step after harvest to avoid rapid degradation of the biomass. In the context of using seaweeds in human food and animal feed products, such practice may affect the nutritional value and the overall quality of the biomass. The effects of seawater storage on the chemical composition (i.e., mineral fraction, carbohydrates, proteins, polyphenols, and fucoxanthin) and surface color of two cultivated kelps (Phaeophyceae), Alaria esculenta and Saccharina latissima, were investigated over a 22-h period. Storage treatments resulted in a rapid decrease in dry weight during the first 2 h (−21.4 and −20.4% in A. esculenta and S. latissima, respectively) with subsequent stabilization. Although it is not clear whether the reduction of dry weight was caused by the release of nutritional compounds from seaweed biomass or water uptake during storage treatment, the results from chemical analyses suggest the combined effect of both mechanisms. Seawater storage increased the ash and sodium contents and reduced carbohydrate and polyphenol levels in both species. Among carbohydrates, the levels of mannitol and glucose (laminaran) were particularly reduced in S. latissima samples while the fucose level, reflecting fucoidans, was reduced in A. esculenta. The protein content remained relatively stable in both species. These results provide evidence of the effect of seawater storage on the quality of the edible kelps A. esculenta and S. latissima. The results will contribute to selecting postharvest strategies adequate for maintaining biomass quality, minimizing losses of valuable compounds and increasing profitability for industrial stakeholders.

Keywords

Alginate Bioactive compounds Carbohydrates Chemical composition analysis Edible seaweeds Fucose Fucoxanthin Laminaran Macroalgae Mannitol Minerals Polyphenols Potassium Preservation Processing Protein Sodium 

Notes

Acknowledgements

This work was conducted as part of the PROMAC project (244244), funded by the Research Council of Norway and part of the Sustainable Innovation in Food- and Bio-based Industries Programme. Pierrick Stévant was supported by a doctoral fellowship from Sparebanken Møre. The authors are also grateful to two anonymous reviewers for their valuable comments and contribution in improving the manuscript.

References

  1. Abdullah MI, Fredriksen S (2004) Production, respiration and exudation of dissolved organic matter by the kelp Laminaria hyperborea along the west coast of Norway. J Mar Biol Assoc UK 84:887–894CrossRefGoogle Scholar
  2. Adams JMM, Ross AB, Anastasakis K, Hodgson EM, Gallagher JA, Jones JM, Donnison IS (2011) Seasonal variation in the chemical composition of the bioenergy feedstock Laminaria digitata for thermochemical conversion. Bioresour Technol 102:226–234CrossRefPubMedGoogle Scholar
  3. Adams JMM, Schmidt A, Gallagher JA (2014) The impact of sample preparation of the macroalgae Laminaria digitata on the production of the biofuels bioethanol and biomethane. J Appl Phycol 27:985–991CrossRefGoogle Scholar
  4. AFNOR (1977) Norme NF V18–101: aliments des animaux - Dosage des cendres brutesGoogle Scholar
  5. Ale MT, Maruyama H, Tamauchi H, Mikkelsen JD and Meyer AS (2011) Fucose-containing sulfated polysaccharides from brown seaweeds inhibit proliferation of melanoma cells and induce apoptosis by activation of caspase-3 in vitro. Mar Drugs 9(12):2605Google Scholar
  6. Angell AR, Mata L, de Nys R, Paul NA (2016) The protein content of seaweeds: a universal nitrogen-to-protein conversion factor of five. J Appl Phycol 28:511–524CrossRefGoogle Scholar
  7. AOAC Iternational (2000) Official methods of analysis of AOAC international, 17th edn. Association of Official Analytical Chemistry, MarylandGoogle Scholar
  8. Baghel RS, Trivedi N, Reddy CRK (2016) A simple process for recovery of a stream of products from marine macroalgal biomass. Bioresour Technol 203:160–165CrossRefPubMedGoogle Scholar
  9. Bischof K, Rautenberger R (2012) Seaweed responses to environmental stress: reactive oxygen and antioxidative strategies. In: Wiencke C, Bischof K (eds) Seaweed biology: novel insights into ecophysiology, ecology and utilization. Springer, Berlin, pp 109–132CrossRefGoogle Scholar
  10. Black W (1950) The seasonal variation in weight and chemical composition of the common British Laminariaceae. J Mar Biol Assoc UK 29:45–72CrossRefGoogle Scholar
  11. Brinkhuis BH, Levine HG, Schlenk CG, Tobin S (1987) Laminaria cultivation in the far east and North America. In: Bird KT, Benson PH (eds) Seaweed cultivation for renewable resources. Development in aquaculture and fisheries science. Elsevier, New York, pp 107–146Google Scholar
  12. Brownlee IA, Allen A, Pearson JP, Dettmar PW, Havler ME, Atherton MR, Onsøyen E (2005) Alginate as a source of dietary fiber. Crit Rev Food Sci 45:497–510CrossRefGoogle Scholar
  13. Bruhn A, Tørring DB, Thomsen M, Canal-Vergés P, Nielsen MM, Rasmussen MB, Eybye KL, Larsen MM, Balsby TJS, Petersen JK (2016) Impact of environmental conditions on biomass yield, quality, and bio-mitigation capacity of Saccharina latissima. Aquac Environ Interac 8:619–636CrossRefGoogle Scholar
  14. Burritt DJ, Larkindale J, Hurd CL (2002) Antioxidant metabolism in the intertidal red seaweed Stictosiphonia arbuscula following desiccation. Planta 215:829–838CrossRefPubMedGoogle Scholar
  15. Cabrita ARJ, Maia MRG, Oliveira HM, Sousa-Pinto I, Almeida AA, Pinto E, Fonseca AJM (2016) Tracing seaweeds as mineral sources for farm-animals. J Appl Phycol 28:3135–3150CrossRefGoogle Scholar
  16. Chan JCC, Cheung PCK, Ang PO (1997) Comparative studies on the effect of three drying methods on the nutritional composition of seaweed Sargassum hemiphyllum (Turn.) C. Ag. J Agr Food Chem 45:3056–3059CrossRefGoogle Scholar
  17. Chapman AS, Stévant P, Emblem Larssen W (2015) Food or fad? Challenges and opportunities for including seaweeds in a Nordic diet. Bot Mar 58:423–433CrossRefGoogle Scholar
  18. Connan S, Delisle F, Deslandes E, Ar Gall E (2006) Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters. Bot Mar 49:39–46CrossRefGoogle Scholar
  19. Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem 103:891–899CrossRefGoogle Scholar
  20. Déléris P, Nazih H, Bard JM (2016) Seaweeds in human health. In: Fleurence J, Levine I (eds) Seaweed in health and disease prevention. Academic Press, Elsevier, Amsterdam, pp 319–367CrossRefGoogle Scholar
  21. Draget KI, Smidsrød O, Skjåk Bræk G (2002) Alginates from algae. In: De Baets S, Vandamme EJ, Steinbuchel A (eds) Biopolymers. Wiley, Weinheim, pp 215–244Google Scholar
  22. Enríquez S, Duarte CM, Sand-Jensen K (1993) Patterns in decomposition rates among photosynthetic organisms: the importance of detritus C: N: P content. Oecologia 94:457–471CrossRefPubMedGoogle Scholar
  23. Evans FD, Critchley AT (2014) Seaweeds for animal production use. J Appl Phycol 26:891–899CrossRefGoogle Scholar
  24. Fleurence J (2004) Seaweed proteins. In: Yada RY (ed) Proteins in food processing. Woodhead Publishing, Cambridge, pp 197–213CrossRefGoogle Scholar
  25. Fleurence J, Ar Gall E (2016) Antiallergic properties. In: Fleurance J, Levine I (eds) Seaweed in health and disease prevention. Academic Press, Elsevier, Amsterdam, pp 389–406CrossRefGoogle Scholar
  26. Flores-Molina MR, Thomas D, Lovazzano C, Núñez A, Zapata J, Kumar M, Correa JA, Contreras-Porcia L (2014) Desiccation stress in intertidal seaweeds: effects on morphology, antioxidant responses and photosynthetic performance. Aquat Bot 113:90–99CrossRefGoogle Scholar
  27. Forbord S, Skjermo J, Arff J, Handå A, Reitan KI, Bjerregaard R, Lüning K (2012) Development of Saccharina latissima (Phaeophyceae) kelp hatcheries with year-round production of zoospores and juvenile sporophytes on culture ropes for kelp aquaculture. J Appl Phycol 24:393–399CrossRefGoogle Scholar
  28. Francis FJ (1995) Quality as influenced by color. Food Qual Prefer 6:149–155CrossRefGoogle Scholar
  29. Fung A, Hamid N, Lu J (2013) Fucoxanthin content and antioxidant properties of Undaria pinnatifida. Food Chem 136:1055–1062CrossRefPubMedGoogle Scholar
  30. Girolami A, Napolitano F, Faraone D, Braghieri A (2013) Measurement of meat color using a computer vision system. Meat Sci 93:111–118CrossRefPubMedGoogle Scholar
  31. Guiné RPF, Barroca MJ (2012) Effect of drying treatments on texture and color of vegetables (pumpkin and green pepper). Food Bioprod Process 90:58–63CrossRefGoogle Scholar
  32. Gupta S, Cox S, Abu-Ghannam N (2011) Effect of different drying temperatures on the moisture and phytochemical constituents of edible Irish brown seaweed. LWT - Food Sci Technol 44:1266–1272CrossRefGoogle Scholar
  33. Handå A, Forbord S, Wang X, Broch OJ, Dahle SW, Størseth TR, Reitan KI, Olsen Y, Skjermo J (2013) Seasonal- and depth-dependent growth of cultivated kelp (Saccharina latissima) in close proximity to salmon (Salmo salar) aquaculture in Norway. Aquaculture 414-415:191–201CrossRefGoogle Scholar
  34. Hayashi K, Nakano T, Hashimoto M, Kanekiyo K, Hayashi T (2008) Defensive effects of a fucoidan from brown alga Undaria pinnatifida against herpes simplex virus infection. Int Immunopharmacol 8:109–116CrossRefPubMedGoogle Scholar
  35. Herrmann C, FitzGerald J, O’Shea R, Xia A, O’Kiely P, Murphy JD (2015) Ensiling of seaweed for a seaweed biofuel industry. Bioresour Technol 196:301–313CrossRefPubMedGoogle Scholar
  36. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  37. Hou X, Hansen JH, Bjerre AB (2015) Integrated bioethanol and protein production from brown seaweed Laminaria digitata. Bioresour Technol 197:310–317CrossRefPubMedGoogle Scholar
  38. Jensen A (1993) Present and future needs for algae and algal products. Hydrobiologia 260:15–23CrossRefGoogle Scholar
  39. Jiménez-Escrig A, Gómez-Ordóñez E, Tenorio MD, Rupérez P (2013) Antioxidant and prebiotic effects of dietary fiber co-travelers from sugar Kombu in healthy rats. J Appl Phycol 25:503–512CrossRefGoogle Scholar
  40. Kanda H, Kamo Y, Machmudah S, Wahyudiono EY, Goto M (2014) Extraction of fucoxanthin from raw macroalgae excluding drying and cell wall disruption by liquefied dimethyl ether. Mar Drugs 12:2383–2396CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kraan S, Verges Tramullas A, Guiry M (2000) The edible brown seaweed Alaria esculenta (Pheophyceae, Laminariales) hybridization growth and genetic comparisons of six Irish populations. J Appl Phycol 12:577–583CrossRefGoogle Scholar
  42. Kumar CS, Ganesan P, Suresh PV, Bhaskar N (2008) Seaweeds as a source of nutritionally beneficial compounds. J Food Sci Tech Mys 45:1–13Google Scholar
  43. Liot F, Colin A, Mabeau S (1993) Microbiology and storage life of fresh edible seaweeds. J Appl Phycol 5:243–247CrossRefGoogle Scholar
  44. López-López I, Bastida S, Ruiz-Capillas C, Bravo L, Larrea MT, Sánchez-Muniz F, Cofrades S, Jiménez-Colmenero F (2009a) Composition and antioxidant capacity of low-salt meat emulsion model systems containing edible seaweeds. Meat Sci 83:492–498CrossRefPubMedGoogle Scholar
  45. López-López I, Cofrades S, Ruiz-Capillas C, Jiménez-Colmenero F (2009b) Design and nutritional properties of potential functional frankfurters based on lipid formulation, added seaweed and low salt content. Meat Sci 83:255–262CrossRefPubMedGoogle Scholar
  46. Lourenço SO, Barbarino E, De-Paula JC, da S. Pereira LO, Lanfer Marquez UM (2002) Amino acid composition, protein content and calculation of nitrogen-to-protein conversion factors for 19 tropical seaweeds. Phycol Res 50:233–241CrossRefGoogle Scholar
  47. Mabeau S, Kloareg B, Joseleau J-P (1990) Fractionation and analysis of fucans from brown algae. Phytochemistry 29:2441–2445CrossRefGoogle Scholar
  48. MacArtain P, Gill CIR, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65:535–543CrossRefPubMedGoogle Scholar
  49. Maeda H, Hosokawa M, Sashima T, Funayama K, Miyashita K (2005) Fucoxanthin from edible seaweed, Undaria pinnatifida, shows antiobesity effect through UCP1 expression in white adipose tissues. Biochem Biophys Res Commun 332:392–397CrossRefPubMedGoogle Scholar
  50. Maeda H, Tsukui T, Sashima T, Hosokawa M, Miyashita K (2008) Seaweed carotenoid, fucoxanthin, as a multi-functional nutrient. Asia Pac J Clin Nutr 17(S1):196–199PubMedGoogle Scholar
  51. Mæhre HK, Malde MK, Eilertsen KE, Elvevoll EO (2014) Characterization of protein, lipid and mineral contents in common Norwegian seaweeds and evaluation of their potential as food and feed. J Sci Food Agric 94:3281–3290CrossRefPubMedGoogle Scholar
  52. Magnusson M, Yuen AKL, Zhang R, Wright JT, Taylor RB, Maschmeyer T, de Nys R (2017) A comparative assessment of microwave assisted (MAE) and conventional solid-liquid (SLE) techniques for the extraction of phloroglucinol from brown seaweed. Algal Res 23:28–36CrossRefGoogle Scholar
  53. Mouritsen OG (2016) Those tasty weeds. J Appl Phycol. doi: 10.1007/s10811-016-0986-1:1-6 Google Scholar
  54. Newell R, Lucas M, Velimirov B, Seiderer L (1980) Quantitative significance of dissolved organic losses following fragmentation of kelp Ecklonia maxima and Laminaria pallida. Mar Ecol Prog Ser 2:45–59CrossRefGoogle Scholar
  55. Pádua D, Rocha E, Gargiulo D, Ramos AA (2015) Bioactive compounds from brown seaweeds: phloroglucinol, fucoxanthin and fucoidan as promising therapeutic agents against breast cancer. Phytochem Lett 14:91–98CrossRefGoogle Scholar
  56. Paull RE, Chen NJ (2008) Postharvest handling and storage of the edible red seaweed Gracilaria. Postharvest Biol Tec 48:302–308CrossRefGoogle Scholar
  57. Perez V, Chang ET (2014) Sodium-to-potassium ratio and blood pressure, hypertension, and related factors. Adv Nutr 5:712–741CrossRefPubMedPubMedCentralGoogle Scholar
  58. Quemener B, Marot C, Mouillet L, Da Riz V, Diris J (2000) Quantitative analysis of hydrocolloids in food systems by methanolysis coupled to reverse HPLC. Part 1. Gelling carrageenans. Food Hydrocolloid 14:9–17CrossRefGoogle Scholar
  59. Quitain AT, Kai T, Sasaki M, Goto M (2013) Supercritical carbon dioxide extraction of fucoxanthin from Undaria pinnatifida. J Agr Food Chem 61:5792–5797CrossRefGoogle Scholar
  60. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org Google Scholar
  61. Ragan MA, Glombitza KW (1986) Phlorotannins, brown algal polyphenols. Prog Phycol Res 4:130–230Google Scholar
  62. Rupérez P (2002) Mineral content of edible marine seaweeds. Food Chem 79:23–26CrossRefGoogle Scholar
  63. Rupérez P, Saura-Calixto F (2001) Dietary fibre and physicochemical properties of edible Spanish seaweeds. Eur Food Res Technol 212:349–354CrossRefGoogle Scholar
  64. Sánchez-Machado DI, López-Cervantes J, López-Hernández J, Paseiro-Losada P (2004) Fatty acids, total lipid, protein and ash contents of processed edible seaweeds. Food Chem 85:439–444CrossRefGoogle Scholar
  65. Schiener P, Black KD, Stanley MS, Green DH (2015) The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol 27:363–373CrossRefGoogle Scholar
  66. Skriptsova AV (2015) Fucoidans of brown algae: biosynthesis, localization, and physiological role in thallus. Russ J Mar Biol 41:145–156CrossRefGoogle Scholar
  67. Soler-Vila A, Coughlan S, Guiry M, Kraan S (2009) The red alga Porphyra dioica as a fish-feed ingredient for rainbow trout effects on growth, feed efficiency and carcass composition. J Appl Phycol 21:617–624CrossRefGoogle Scholar
  68. Wang T, Jónsdóttir R, Ólafsdóttir G (2009) Total phenolic compounds, radical scavenging and metal chelation of extracts from Icelandic seaweeds. Food Chem 116:240–248CrossRefGoogle Scholar
  69. Wang T, Jónsdóttir R, Kristinsson HG, Thorkelsson G, Jacobsen C, Hamaguchi PY, Ólafsdóttir G (2010) Inhibition of haemoglobin-mediated lipid oxidation in washed cod muscle and cod protein isolates by Fucus vesiculosus extract and fractions. Food Chem 123:321–330CrossRefGoogle Scholar
  70. Yam KL, Papadakis SE (2004) A simple digital imaging method for measuring and analyzing color of food surfaces. J Food Eng 61:137–142CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.Møreforsking Ålesund ASÅlesundNorway
  2. 2.The Norwegian University of Science and Technology NTNUTrondheimNorway
  3. 3.CEVA (Centre d’Etude et de Valorisation des Algues)PleubianFrance
  4. 4.SINTEF Materials and ChemistryTrondheimNorway
  5. 5.MMS (Mer Molécule Santé)Université de NantesNantes cedex 3France

Personalised recommendations