Seaweed as a protein source for mono-gastric livestock

Trends in Food Science and Technology

Volumn 54, Issue , 2016, Pages 74-84

  Angell, Alex R ^a   Angell, Simon F ^b   de Nys, Rocky ^a   Paul, Nicholas A ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BENCHMARKING; PROTEINS; SEAWEED;

AGRICULTURAL RESOURCES; ALTERNATIVE SOURCE; ESSENTIAL AMINO ACIDS; GLOBAL DISTRIBUTION; LIVESTOCK FEED; NUTRITIONAL PROFILES; PROTEIN SOURCES; TOTAL AMINO ACIDS;

AGRICULTURE;

EID: 84973299885     PISSN: 09242244     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tifs.2016.05.014     Document Type: Review

References (98)

1. Abudabos A.M., Okab A.B., Aljumaah R.S., Samara E.M., Abdoun K.A., Al-Haidary A.A. Nutritional value of green seaweed (Ulva lactuca) for broiler chickens. Italian Journal of Animal Science 2013, 12.
2. Agboola S., Ng D., Mills D. Characterisation and functional properties of Australian rice protein isolates. Journal of cereal science 2005, 41:283-290.
3. Aiking H. Future protein supply. Trends in Food Science & Technology 2011, 22:112-120.
4. Al-Harthi M.A., El-Deek A.A. Nutrient profiles of brown marine algae (Sargassum dentifebium) as affected by different processing methods for chickens. Journal of Food Agriculture Environment 2012, 10:475-480.
5. Alves A., Sousa R.A., Reis R.L. A practical perspective on ulvan extracted from green algae. Journal of Applied Phycology 2013, 25:407-424.
6. Angell A.R., de Nys R., Paul N.A. The nitrogen, protein and amino acid content of seaweeds 2015, [data set]. 10.4225/28/55776D6F45871.
7. Angell A.R., Mata L., de Nys R., Paul N.A. Indirect and direct effects of salinity on the quantity and quality of total amino acids in Ulva ohnoi (Chlorophyta). Journal of Phycology 2015, 51(3):536-545.
8. Angell A.R., Mata L., de Nys R., Paul N.A. The protein content of seaweeds: a universal nitrogen-to-protein conversion factor of five. Journal of Applied Phycology 2016, 28(1):511-524.
9. Araújo M., Rema P., Sousa-Pinto I., Cunha L.M., Peixoto M.J., Pires M.A., et al. Dietary inclusion of IMTA-cultivated Gracilaria vermiculophylla in rainbow trout (Oncorhynchus mykiss) diets: effects on growth, intestinal morphology, tissue pigmentation, and immunological response. Journal of Applied Phycology 2015, 28(1):679-689.
10. Armisen R. World-wide use and importance of Gracilaria. Journal of Applied Phycology 1995, 7:231-243.
11. Asino H., Ai Q.H., Mai K.S. Evaluation of Enteromorpha prolifera as a feed component in large yellow croaker (Pseudosciaena crocea, Richardson, 1846) diets. Aquaculture Research 2011, 42:525-533.
12. Bals B., Dale B.E. Economic comparison of multiple techniques for recovering leaf protein in biomass processing. Biotechnology and Bioengineering 2011, 108:530-537.
13. Barros F.C.N., da Silva D.C., Sombra V.G., Maciel J.S., Feitosa J.P.A., Freitas A.L.P., et al. Structural characterization of polysaccharide obtained from red seaweed Gracilaria caudata (J Agardh). Carbohydrate Polymers 2013, 92:598-603.
14. Bautista-Teruel M.N., Millamena O.M., Fermin A.C. Reproductive performance of hatchery-bred donkey's ear abalone, Haliotis asinina, Linne, fed natural and artificial diets. Aquaculture Research 2001, 32:249-254.
15. Berk Z. Technology of production of edible flours and protein products from soybean 1992, FAO Agricultural Services Bulletin (FAO).
16. Bilbao A., Uriarte I., Viera M.D., Sosa B., Fernandez-Palacios H., Hernandez-Cruz C.M. Effect of macroalgae protein levels on some reproductive aspects and physiological parameters for the abalone, Haliotis tuberculata coccinea (Reeve 1846). Journal of the World Aquaculture Society 2012, 43:764-777.
17. BobinDubigeon C., Lahaye M., Guillon F., Barry J.L., Gallant D.J. Factors limiting the biodegradation of Ulva sp cell-wall polysaccharides. Journal of the Science of Food and Agriculture 1997, 75:341-351.
18. Boland M.J., Rae A.N., Vereijken J.M., Meuwissen M.P., Fischer A.R., van Boekel M.A., et al. The future supply of animal-derived protein for human consumption. Trends in Food Science & Technology 2013, 29:62-73.
19. Bolton J., Robertson-Andersson D., Shuuluka D., Kandjengo L. Growing Ulva (Chlorophyta) in integrated systems as a commercial crop for abalone feed in South Africa: a SWOT analysis. Journal of Applied Phycology 2009, 21:575-583.
20. von Braun J. The world food situation: New driving forces 2007, International Food Policy Research Institute, Washington, DC.
21. Chiesa S., Gnansounou E. Protein extraction from biomass in a bioethanol refinery-Possible dietary applications: use as animal feed and potential extension to human consumption. Bioresource Technology 2011, 102:427-436.
22. Chiovitti A., Bacic A., Craik D.J., Munro S.L., Kraft G.T., Liao M.-L. Cell-wall polysaccharides from Australian red algae of the family Solieriaceae (Gigartinales, Rhodophyta): novel, highly pyruvated carrageenans from the genus Callophycus. Carbohydrate Research 1997, 299:229-243.
23. Cook E.J., Kelly M.S. Effect of variation in the protein value of the red macroalga Palmaria palmata on the feeding, growth and gonad composition of the sea urchins Psammechinus miliaris and Paracentrotus lividus (Echinodermata). Aquaculture 2007, 270:207-217.
24. Cruz-Suarez L.E., Tapia-Salazar M., Nieto-Lopez M.G., Guajardo-Barbosa C., Ricque-Marie D. Comparison of Ulva clathrata and the kelps Macrocystis pyrifera and Ascophyllum nodosum as ingredients in shrimp feeds. Aquaculture Nutrition 2009, 15:421-430.
25. Davies S.J., Brown M.T., Camilleri M. Preliminary assessment of the seaweed Porphyra purpurea in artificial diets for thick-lipped grey mullet (Chelon labrosus). Aquaculture 1997, 152:249-258.
26. Dierick N., Ovyn A., De Smet S. Effect of feeding intact brown seaweed Ascophyllum nodosum on some digestive parameters and on iodine content in edible tissues in pigs. Journal of the Science of Food and Agriculture 2009, 89:584-594.
27. El-Deek A., Brikaa A.M. Effect of different levels of seaweed in starter and finisher diets in pellet and mash form on performance and carcass quality of ducks. International Journal Poultry Science 2009, 8:1014-1021.
28. El-Deek A., Brikaa M.A. Nutritional and biological evaluation of marine seaweed as a feedstuff and as a pellet binder in poultry diet. International Journal of Poultry Science 2009, 8:875-881.
29. Ellis R.J. The most abundant protein in the world. Trends in Biochemical Sciences 1979, 4:241-244.
30. Felix N., Brindo R.A. Substituting fish meal with fermented seaweed, Kappaphycus alvarezii in diets of juvenile freshwater prawn Macrobrachium rosenbergii. International Journal of Fisheries and Aquatic Studies 2013, 1.
31. Fleurence J. Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends in Food Science & Technology 1999, 10:25-28.
32. Fleurence J., LeCoeur C., Mabeau S., Maurice M., Landrein A. Comparison of different extractive procedures for proteins from the edible seaweeds Ulva rigida and Ulva rotundata. Journal of Applied Phycology 1995, 7:577-582.
33. Fleurence J., Morancais M., Dumay J., Decottignies P., Turpin V., Munier M., et al. What are the prospects for using seaweed in human nutrition and for marine animals raised through aquaculture?. Trends in Food Science & Technology 2012, 27:57-61.
34. Garcia-Vaquero M., Hayes M. Red and Green Macroalgae for fish, animal feed and human functional food development. Food Reviews International 2015, 32(1):15-45.
35. Godfray H.C.J., Beddington J.R., Crute I.R., Haddad L., Lawrence D., Muir J.F., et al. Food security: the challenge of feeding 9 billion people. Science 2010, 327:812-818.
36. Harnedy P.A., FitzGerald R.J. Bioactive proteins, peptides, and amino acids from macroalgae. Journal of Phycology 2011, 47:218-232.
37. Holdt S., Kraan S. Bioactive compounds in seaweed: functional food applications and legislation. Journal of Applied Phycology 2011, 23:543-597.
38. Jordan P., Vilter H. Extraction of proteins from material rich in anionic mucilages: partition and fractionation of vanadate-dependent bromoperoxidases from the brown algae Laminaria digitata and L. saccharina in aqueous polymer two-phase systems. Biochimica et Biophysica Acta (BBA)-General Subjects 1991, 1073:98-106.
39. Ju Z., Hettiarachchy N., Rath N. Extraction, denaturation and hydrophobic properties of rice flour proteins. Journal of Food Science 2001, 66:229-232.
40. Kandasamy G., Karuppiah S.K., Rao P.V.S. Salt- and pH-induced functional changes in protein concentrate of edible green seaweed Enteromorpha species. Fisheries Science 2012, 78:169-176.
41. Katayama M., Fukuda T., Okamura T., Suzuki E., Tamura K., Shimizu Y., et al. Effect of dietary addition of seaweed and licorice on the immune performance of pigs. Animal Science Journal 2011, 82:274-281.
42. Kemp J.O.G., Britz P.J., Aguero P.H.T. The effect of macroalgal, formulated and combination diets on growth, survival and feed utilisation in the red abalone Haliotis rufescens. Aquaculture 2015, 448:306-314.
43. Kolender A.A., Matulewicz M.C. Sulfated polysaccharides from the red seaweed Georgiella confluens. Carbohydrate Research 2002, 337:57-68.
44. Kraan S. Algal polysaccharides, novel applications and outlook 2012, INTECH Open Access Publisher.
45. Kulshreshtha G., Rathgeber B., Stratton G., Thomas N., Evans F., Critchley A., et al. Feed supplementation with red seaweeds, Chondrus crispus and Sarcodiotheca gaudichaudii, affects performance, egg quality, and gut microbiota of layer hens. Poultry Science 2014, 93:2991-3001.
46. Kumar K.S., Ganesan K., Selvaraj K., Rao P.V.S. Studies on the functional properties of protein concentrate of Kappaphycus alvarezii (Doty) Doty - an edible seaweed. Food Chemistry 2014, 153:353-360.
47. Leser S. The 2013 FAO report on dietary protein quality evaluation in human nutrition: Recommendations and implications. Nutrition Bulletin 2013, 38:421-428.
48. Loomis W.D., Battaile J. Plant phenolic compounds and the isolation of plant enzymes. Phytochemistry 1966, 5:423-438.
49. Mabeau S., Fleurence J. Seaweed in food-products - biochemical and nutritional aspects. Trends in Food Science & Technology 1993, 4:103-107.
50. Maciel J.S., Chaves L.S., Souza B.W.S., Teixeira D.I.A., Freitas A.L.P., Feitosa J.P.A., et al. Structural characterization of cold extracted fraction of soluble sulfated polysaccharide from red seaweed Gracilaria birdiae. Carbohydrate Polymers 2008, 71:559-565.
51. Magnusson M., Carl C., Mata L., de Nys R., Paul N.A. Seaweed salt from Ulva: a novel first step in a cascading biorefinery model. Algal Research 2016, 16:308-316.
52. Marinho G., Nunes C., Sousa-Pinto I., Pereira R., Rema P., Valente L.M.P. The IMTA-cultivated Chlorophyta Ulva spp. as a sustainable ingredient in Nile tilapia (Oreochromis niloticus) diets. Journal of Applied Phycology 2013, 25:1359-1367.
53. Marrion O., Fleurence J., Schwertz A., Guéant J.-L., Mamelouk L., Ksouri J., et al. Evaluation of protein in vitro digestibility of Palmaria palmata and Gracilaria verrucosa. Journal of Applied Phycology 2005, 17:99-102.
54. Mata L., Magnusson M., Paul N.A., de Nys R. The intensive land-based production of the green seaweeds Derbesia tenuissima and Ulva ohnoi: biomass and bioproducts. Journal of Applied Phycology 2016, 28(1):365-375.
55. Mata L., Schuenhoff A., Santos R. A direct comparison of the performance of the seaweed biofilters, Asparagopsis armata and Ulva rigida. Journal of Applied Phycology 2010, 22:639-644.
56. McDermid K.J., Stuercke B. Nutritional composition of edible Hawaiian seaweeds. Journal of Applied Phycology 2003, 15:513-524.
57. McDermid K.J., Stuercke B., Balazs G.H. Nutritional composition of marine plants in the diet of the green sea turtle (Chelonia mydas) in the Hawaiian Islands. Bulletin of Marine Science 2007, 81:55-71.
58. Melo M.R.S., Feitosa J.P.A., Freitas A.L.P., de Paula R.C.M. Isolation and characterization of soluble sulfated polysaccharide from the red seaweed Gracilaria cornea. Carbohydrate Polymers 2002, 49:491-498.
59. Michalak I., Chojnacka K., Dobrzanski Z., Gorecki H., Zielinska A., Korczynski M., et al. Effect of macroalgae enriched with microelements on egg quality parameters and mineral content of eggs, eggshell, blood, feathers and droppings. Journal of Animal Physiology and Animal Nutrition 2011, 95:374-387.
60. Moroney N.C., Wan A.H.L., Soler-Vila A., FitzGerald R.D., Johnson M.P., Kerry J.P. Inclusion of Palmaria palmata (red seaweed) in Atlantic salmon diets: effects on the quality, shelf-life parameters and sensory properties of fresh and cooked salmon fillets. Journal of the Science of Food and Agriculture 2015, 95:897-905.
61. Mulvaney W.J., Winberg P.C., Adams L. Comparison of macroalgal (Ulva and Grateloupia spp.) and formulated terrestrial feed on the growth and condition of juvenile abalone. Journal of Applied Phycology 2013, 25:815-824.
62. Neveux N., Yuen A., Jazrawi C., He Y., Magnusson M., Haynes B., et al. Pre-and post-harvest treatment of macroalgae to improve the quality of feedstock for hydrothermal liquefaction. Algal Research 2014, 6:22-31.
63. Nielsen M.M., Bruhn A., Rasmussen M.B., Olesen B., Larsen M.M., Moller H.B. Cultivation of Ulva lactuca with manure for simultaneous bioremediation and biomass production. Journal of Applied Phycology 2012, 24:449-458.
64. Nigam P.S., Singh A. Production of liquid biofuels from renewable resources. Progress in Energy and Combustion Science 2011, 37:52-68.
65. NRC Nutrient requirements of poultry 1994, The National Academy Press, Washington, DC.
66. NRC Nutrient requirements of swine 1998, The National Academy Press, Washington, DC.
67. NRC Nutrient requirements of fish and shrimp 2011, National Academy Press, Washington, DC.
68. NRC Nutrient requirements of swine 2012, The National Academy Press, Washington, DC.
69. Percival E. The polysaccharides of green, red and brown seaweeds: their basic structure, biosynthesis and function. British Phycological Journal 1979, 14:103-117.
70. Pereira R., Valente L.M.P., Sousa-Pinto I., Rema P. Apparent nutrient digestibility of seaweeds by rainbow trout (Oncorhynchus mykiss) and Nile tilapia (Oreochromis niloticus). Algal Research-Biomass Biofuels and Bioproducts 2012, 1:77-82.
71. Pretty J. Agricultural sustainability: concepts, principles and evidence. Philosophical Transactions of the Royal Society B-Biological Sciences 2008, 363:447-465.
72. Ragaza J.A., Koshio S., Mamauag R.E., Ishikawa M., Yokoyama S., Villamor S.S. Dietary supplemental effects of red seaweed Eucheuma denticulatum on growth performance, carcass composition and blood chemistry of juvenile Japanese flounder, Paralichthys olivaceus. Aquaculture Research 2015, 46:647-657.
73. Ray B. Polysaccharides from Enteromorpha compressa: isolation, purification and structural features. Carbohydrate Polymers 2006, 66:408-416.
74. Ray B., Lahaye M. Cell-wall polysaccharides from the marine green-alga Ulva rigida (Ulvales, Chlorophyta) - extraction and chemical-composition. Carbohydrate Research 1995, 274:251-261.
75. Shapawi R., Safiin N.S.Z., Senoo S. Improving dietary red seaweed Kappaphycus alvarezii (Doty) Doty ex. P. Silva meal utilization in Asian seabass Lates calcarifer. Journal of Applied Phycology 2015, 27:1681-1688.
76. Shapawi R., Zamry A.A. Response of Asian seabass, Lates calcarifer juvenile fed with different seaweed-based diets. Journal of Applied Animal Research 2016, 44:121-125.
77. da Silva R.L., Barbosa J.M. Seaweed meal as a protein source for the white shrimp Litopenaeus vannamei. Journal of Applied Phycology 2009, 21:193-197.
78. Sinclair S. Protein extraction from pasture. Literature review Part A: The plant fractionation bio-porcess and adaptability to farming systems 2009, 8. Milestone Report prepared for MAF SFF Grant C.
79. Spreitzer R.J., Salvucci M.E. Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Plant Biology 2002, 53.
80. Stadtlander T., Khalil W.K.B., Focken U., Becker K. Effects of low and medium levels of red alga Nori (Porphyra yezoensis Ueda) in the diets on growth, feed utilization and metabolism in intensively fed Nile tilapia, Oreochromis niloticus (L.). Aquaculture Nutrition 2013, 19:64-73.
81. Stein H., Seve B., Fuller M., Moughan P., De Lange C. Invited review: amino acid bioavailability and digestibility in pig feed ingredients: terminology and application. Journal of Animal Science 2007, 85:172.
82. Tacon A.G.J., Metian M. Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 2008, 285:146-158.
83. Tan S.H., Mailer R.J., Blanchard C.L., Agboola S.O. Canola proteins for human consumption: extraction, profile, and functional properties. Journal of Food Science 2011, 76:R16-R28.
84. Valente L.M.P., Gouveia A., Rema P., Matos J., Gomes E.F., Pinto I.S. Evaluation of three seaweeds Gracilaria bursa-pastoris, Ulva rigida and Gracilaria cornea as dietary ingredients in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 2006, 252:85-91.
85. Valente L.M.P., Rema P., Ferraro V., Pintado M., Sousa-Pinto I., Cunha L.M., et al. Iodine enrichment of rainbow trout flesh by dietary supplementation with the red seaweed Gracilaria vermiculophylla. Aquaculture 2015, 446:132-139.
86. Ventura M.R., Castanon J.I.R., Mcnab J.M. Nutritional-value of seaweed (Ulva rigida) for poultry. Animal Feed Science and Technology 1994, 49:87-92.
87. Viera M.P., de Vicose G.C., Gomez-Pinchetti J.L., Bilbao A., Fernandez-Palacios H., Izquierdo M.S. Comparative performances of juvenile abalone (Haliotis tuberculata coccinea Reeve) fed enriched vs non-enriched macroalgae: effect on growth and body composition. Aquaculture 2011, 319:423-429.
88. Walker A.B., Fournier H.R., Neefus C.D., Nardi G.C., Berlinsky D.L. Partial replacement of fish meal with laver Porphyra spp. in diets for Atlantic cod. North American Journal of Aquaculture 2009, 71:39-45.
89. Walsh A.M., Sweeney T., O'Shea C.J., Doyle D.N., O'Doherty J.V. Effect of supplementing varying inclusion levels of laminarin and fucoidan on growth performance, digestibility of diet components, selected faecal microbial populations and volatile fatty acid concentrations in weaned pigs. Animal Feed Science and Technology 2013, 183:151-159.
90. Walsh A.M., Sweeney T., O'Shea C.J., Doyle D.N., O'Doherty J.V. Effect of dietary laminarin and fucoidan on selected microbiota, intestinal morphology and immune status of the newly weaned pig. British Journal of Nutrition 2013, 110:1630-1638.
91. Wassef E.A., El-Sayed A.F.M., Sakr E.M. Pterocladia (Rhodophyta) and Ulva (Chlorophyta) as feed supplements for European seabass, Dicentrarchus labrax L., fry. Journal of Applied Phycology 2013, 25:1369-1376.
92. Wong K., Cheung P.C. Influence of drying treatment on three Sargassum species 2. Protein extractability, in vitro protein digestibility and amino acid profile of protein concentrates. Journal of Applied Phycology 2001, 13:51-58.
93. Wong K.H., Cheung P.C.K. Nutritional evaluation of some subtropical red and green seaweeds Part II. In vitro protein digestibility and amino acid profiles of protein concentrates. Food Chemistry 2001, 72:11-17.
94. Wong K.H., Cheung P.C.K., Ang P.O. Nutritional evaluation of protein concentrates isolated from two red seaweeds: Hypnea charoides and Hypnea japonica in growing rats. Hydrobiologia 2004, 512:271-278.
95. Xu S.D., Zhang L., Wu Q.Y., Liu X.B., Wang S.Q., You C.H., et al. Evaluation of dried seaweed Gracilaria lemaneiformis as an ingredient in diets for teleost fish Siganus canaliculatus. Aquaculture International 2011, 19:1007-1018.
96. Yamamoto M. Physicochemical studies on sulfated polysaccharides extracted from seaweeds at various temperatures. Agricultural and Biological Chemistry 1980, 44:589-593.
97. Yildirim O., Ergun S., Yaman S., Turker A. Effects of two seaweeds (Ulva lactuca and Enteromorpha linza) as a feed additive in diets on growth performance, feed utilization, and body composition of rainbow trout (Oncorhynchus mykiss). Kafkas Universitesi Veteriner Fakultesi Dergisi 2009, 15:455-460.
98. Zahid P.B., Aisha K., Ali A. Green seaweed as component of poultry feed. Bangladesh Journal of Botany 1995, 24:153-156.