Microalgae in aquafeeds for a sustainable aquaculture industry

  • Mahfuzur Rahman Shah
  • Giovanni Antonio Lutzu
  • Asraful Alam
  • Pallab Sarker
  • M. A. Kabir Chowdhury
  • Ali Parsaeimehr
  • Yuanmei Liang
  • Maurycy Daroch
4th AOAIS-Wuhan

Abstract

Due to the rapid global expansion of the aquaculture industry, access to key feedstuffs (fishmeal and fish oil) is becoming increasingly limited because of the finite resources available for wild fish harvesting. This has resulted in other sources of feedstuffs being investigated, namely plant origin substitutes for fishmeal and fish oil for aquafeed. Conventional land-based crops have been favored for some applications as substitutes for a portion of the fishmeal, but they can result in changes in the nutritional quality of the fish produced. Microalgae can be regarded as a promising alternative that can replace fishmeal and fish oil and ensure sustainability standards in aquaculture. They have a potential for use in aquaculture as they are sources of protein, lipid, vitamins, minerals, pigments, etc. This comprehensive review summarizes the most important and recent developments of microalgae use as supplement or feed additive to replace fishmeal and fish oil for use in aquaculture. It also reflects the microalgal nutritional quality and digestibility of microalgae-based aquafeed. Simultaneously, safety and regulatory aspects of microalgae feed applications, major challenges on the use microalgae in aquafeed in commercial production, and future research and development perspective are also presented in a critical manner. This review will serve as a useful guide to present current status of knowledge and highlight key areas for future development of a microalgae-based aquafeed industry and overall development of a sustainable aquaculture industry.

Keywords

Aquaculture Aquafeed fishmeal Fish oil Microalgae Sustainability 

References

  1. Alam MA, Wan C, Zhao XQ, Chen LJ, Chang JS, Bai FW (2015) Enhanced removal of Zn2+ or Cd2+ by the flocculating Chlorella vulgaris JSC-7. J Hazard Mater 289:38–45PubMedCrossRefGoogle Scholar
  2. Allan GL, Parkinson S, Booth MA, Stone DA, Rowland SJ, Frances J, Warner-Smith R (2000) Replacement of fishmeal in diets for Australian silver perch, Bidyanus bidyanus: I. Digestibility of alternative ingredients. Aquaculture 186:293–310CrossRefGoogle Scholar
  3. Ambati RR, Phang SM, Ravi S, Aswathanarayana RG (2014) Astaxanthin: sources, extraction, stability, biological activities and its commercial applications—a review. Mar Drugs 12:128–152PubMedPubMedCentralCrossRefGoogle Scholar
  4. Atack T, Jauncey K, Matty A (1979) The utilization of some single cell proteins by fingerling mirror carp (Cyprinus carpio). Aquaculture 18:337–348CrossRefGoogle Scholar
  5. Atalah E, Cruz CMH, Izquierdo MS, Rosenlund G, Caballero MJ, Valencia A, Robaina L (2007) Two microalgae Crypthecodinium cohnii and Phaeodactylum tricornutum as alternative source of essential fatty acids in starter feeds for seabream (Sparus aurata). Aquaculture 270:178–185CrossRefGoogle Scholar
  6. Badwy TM, Ibrahim EM, Zeinhom MM (2008) Partial replacement of fishmeal with dried microalgae (Chlorella spp. and Scenedesmus spp.) in Nile tilapia (Oreochromis niloticus) diets. In: Elghobashy H, Fitzsimmons K, Diab AS (eds) From the pharaohs to the future: proceedings of the 8th international symposium on tilapia in aquaculture. Egypt Ministry of Agriculture, Cairo, pp 801–810Google Scholar
  7. Barclay W, Zeller S (1996) Nutritional enhancement of n-3 and n-6 fatty acids in rotifers and Artemia nauplii by feeding spray-dried Schizochytrium sp. J World Aquacult Soc 27:314–322CrossRefGoogle Scholar
  8. Basri NA, Shaleh SRM, Matanjun P, Noor NM, Shapawi R (2015) The potential of microalgae meal as an ingredient in the diets of early juvenile Pacific white shrimp, Litopenaeus vannamei. J Appl Phycol 27:857–863CrossRefGoogle Scholar
  9. Becker E (2007) Micro-algae as a source of protein. Biotechnol Adv 25:207–210PubMedCrossRefGoogle Scholar
  10. Becker EW (1994) Microalgae: biotechnology and microbiology. Cambridge University Press, Cambridge, 293pGoogle Scholar
  11. Becker W (2004) Microalgae in human and animal nutrition. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Science Ltd, Cambridge, pp 312–351Google Scholar
  12. Benemann J (2013). Microalgae for biofules and animal feeds. Energies 6:5869–5886Google Scholar
  13. Berge G, Hatlen B, Odom J, Ruyter B (2013) Physical treatment of high EPA Yarrowia lipolytica biomass increases the availability of n- 3 highly unsaturated fatty acids when fed to Atlantic salmon. Aquac Nutr 19:110–121CrossRefGoogle Scholar
  14. Bigogno C, Khozin-Goldberg I, Boussiba S, Vonshak A, Cohen Z (2002) Lipid and fatty acid composition of the green oleaginous alga Parietochloris incisa, the richest plant source of arachidonic acid. Phytochemistry 60:497–503PubMedCrossRefGoogle Scholar
  15. Blazencic J (2007) Sistematika algi. NNK Internacional, BeogradGoogle Scholar
  16. Boonyaratpalin M, Thongrod S, Supamattaya K, Britton G, Schlipalius LE (2001) Effects of ß-carotene source, Dunaliella salina, and astaxanthin on pigmentation, growth, survival and health of Penaeus monodon. Aquac Res 32(Suppl 1):182–190CrossRefGoogle Scholar
  17. Borowitzka MA (2013a) High-value products from microalgae-their development and commercialisation. J Appl Phycol 25:743–756CrossRefGoogle Scholar
  18. Borowitzka MA (2013b) Dunaliella: biology, production, and markets. In: Richmond A, Hu Q (eds) Handbook of microalgal culture. John Wiley & Sons, Ltd, pp 359–368CrossRefGoogle Scholar
  19. Bowen SH (1976). Feeding ecology of the cichlid fish Sarotherodon mossambicus in Lake Sibaya, KwaZulu. Doctoral dissertation, Rhodes University, Grahamstown, South AfricaGoogle Scholar
  20. Brown M, Jeffrey S, Volkman J, Dunstan G (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151:315–331CrossRefGoogle Scholar
  21. Brown MR (2002) Nutritional value and use of microalgae in aquaculture. In: Avances en Nutrición Acuícola VI. Memorias del VI Simposium Internacional de Nutrición Acuícola, vol 3, pp 281–292Google Scholar
  22. Brown MR, Jeffry SW (1992) Biochemical composition of microalgae from the green algal classes Chlorophyceae and Prasinophyceae. 1. Amino acids, sugars and pigments. J Exp Mar Biol Ecol 161:91–113CrossRefGoogle Scholar
  23. Burr GS, Wolters WR, Barrows FT, Hardy RW (2012) Replacing fishmeal with blends of alternative proteins on growth performance of rainbow trout (Oncorhynchus mykiss), and early or late stage juvenile Atlantic salmon (Salmo salar). Aquaculture 334:110–116CrossRefGoogle Scholar
  24. Carter CG, Bransden MP, Lewis TE, Nichols PD (2003) Potential of Thraustochytrids to partially replace fish oil in Atlantic salmon feeds. Mar Biotechnol 5:480–492PubMedCrossRefGoogle Scholar
  25. Carvalho YBM, Ferreira JF, Da Silva FC, Bercht M (2013) Factors influencing larval settlement of the Atlantic lion's paw scallop, Nodipecten nodosus. J Shellfish Res 32:719–723CrossRefGoogle Scholar
  26. Cerezuela R, Guardiola FA, Meseguer J, Esteban MA (2012) Enrichment of gilthead seabream (Sparus aurata L.) diet with microalgae: effects on the immune system. Fish Physiol Biochem 38:1729–1739PubMedCrossRefGoogle Scholar
  27. Ceron-Garcia M, Fernandez-Sevilla J, Sanchez-Miron A, Garcia-Camacho F, Contreras-Gomez A, Molina-Grima E (2013) Mixotrophic growth of Phaeodactylum tricornutum on fructose and glycerol in fed-batch and semi-continuous modes. Bioresour Technol 147:569–576PubMedCrossRefGoogle Scholar
  28. Chatzifotis S, Pavlidis M, Jimeno CD, Vardanis G, Sterioti A, Divanach P (2005) The effect of different carotenoid sources on skin coloration of cultured red porgy (Pagrus pagrus). Aquac Res 36:1517–1525CrossRefGoogle Scholar
  29. Chauton MS, Reitan KI, Norsker NH, Tveterås R, Kleivdal HT (2015) A techno-economic analysis of industrial production of marine microalgae as a source of EPA and DHA-rich raw material for aquafeed: research challenges and possibilities. Aquaculture 436:95–103CrossRefGoogle Scholar
  30. Chen CY, Chen YC, Huang HC, Ho SH, Chang JS (2015) Enhancing the production of eicosapentaenoic acid (EPA) from Nannochloropsis oceanica CY2 using innovative photobioreactors with optimal light source arrangements. Bioresour Technol 191:407–413PubMedCrossRefGoogle Scholar
  31. Chen S, Chi Z, O’Fallon JV, Zheng Y, Chakraborty M, Laskar DD (2010) System integration for producing microalgae as biofuel feedstock. Biofuels 1:889–910CrossRefGoogle Scholar
  32. Dallaire V, Lessard P, Vandenberg G, de la Noüe J (2007) Effect of algal incorporation on growth, survival and carcass composition of rainbow trout (Oncorhynchus mykiss) fry. Bioresour Technol 98:1433–1439PubMedCrossRefGoogle Scholar
  33. Daroch M, Shao C, Liu Y, Geng S, Cheng JJ (2013) Induction of lipids and resultant FAME profiles of microalgae from coastal waters of Pearl River Delta. Bioresour Technol 146:192–199PubMedCrossRefGoogle Scholar
  34. Das BK, Pradhan J, Sahu S (2009) The effect of Euglena viridis on immune response of rohu, Labeo rohita (Ham.) Fish Shellfish Immunol 26:871–876PubMedCrossRefGoogle Scholar
  35. Davis R, Aden A, Pienkos PT (2011) Techno-economic analysis of autotrophic microalgae for fuel production. Appl Energ 88:3524–3531CrossRefGoogle Scholar
  36. Draganovic V, Jørgensen SE, Boom R, Riese G, van der Goot AJ (2013) Sustainability assessment of salmonid feed using energy, classical exergy and eco-exergy analysis. Ecol Indic 34:277–289CrossRefGoogle Scholar
  37. Ekpo I, Bender J (1989) Digestibility of a commercial fish feed, wet algae, and dried algae by Tilapia nilotica and silver carp. Prog Fish Cult 51:83–86CrossRefGoogle Scholar
  38. El-Sayed AFM (1994) Evaluation of soybean meal, Spirulina meal and chicken offal meal as protein sources for silver seabream (Rhabdosargus sarba) fingerlings. Aquaculture 127:169–176CrossRefGoogle Scholar
  39. Enzing C, Ploeg M, Barbosa M, Sijtsma L (2014) Microalgae-based products for the food and feed sector: an outlook for Europe. In: Vigani M, Parisi C, Rodríguez Cerezo E (eds). JRC Scientific and Policy Reports, EU Publications: Luxembourg. 82pGoogle Scholar
  40. Enzing, CM, Nooijen A, Eggink G, Springer J, Wijffels R (2012) Algae and genetic modification. Research, production and risks. http://www.cogem.net/index. cfm/nl/publicaties/publicatie/onderzoeksrapport-algae-andgenetic-modification-research-production-and-risks
  41. FAO (2007) The state of world fisheries and aquaculture. FAO, Rome. (http://www.fao.org/docrep/fao/009/a0699e/a0699e.pdf )
  42. FAO (2012) The state of world fisheries and aquaculture. FAO, Rome. (http://www.fao.org/docrep/016/i2727e/i2727e.pdf)Google Scholar
  43. FAO (2014) The state of world fisheries and aquaculture: opportunities and challenges. FAO, Rome. (http://www.fao.org/3/a-i3720e.pdf )
  44. FAO (2016) The state of world fisheries and aquaculture 2016. Contributing to food security and nutrition for all. Rome. 200 pp. (http://www.fao.org/3/a-i5555e.pdf )
  45. FDA (2010) http://www.fda.gov/regulatoryinformation/legislation/federal food drug and cosmetic act fdcact/default. html)
  46. Ganuza E, Benítez-Santana T, Atalah E, Vega-Orellana O, Ganga R, Izquierdo M (2008) Crypthecodinium cohnii and Schizochytrium sp. as potential substitutes to fisheries-derived oils from seabream (Sparus aurata) microdiets. Aquaculture 277:109–116CrossRefGoogle Scholar
  47. Gong Y, Guterres HADS, Huntley M, Sørensen M, Kiron V (2017) Digestibility of the defatted microalgae Nannochloropsis sp. and Desmodesmus sp. when fed to Atlantic salmon, Salmo salar. Aquacult Nutr doi:10.1111/anu.12533
  48. Guedes AC, Malcata FX (2012) Nutritional value and uses of microalgae in aquaculture. In: Muchlisin Z (ed) Aquaculture. INTECH, Riejeka, pp 59–78Google Scholar
  49. Guschina IA, Harwood JL (2013) Algal lipids and their metabolism. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy. Springer, Dordrecht, pp 17–36CrossRefGoogle Scholar
  50. Haas S, Bauer JL, Adakli A, Meyer S, Lippemeier S, Schwarz K, Schulz C (2016) Marine microalgae Pavlova viridis and Nannochloropsis sp. as n-3 PUFA source in diets for juvenile European sea bass (Dicentrarchus labrax L.) J Appl Phycol 28: 1011Google Scholar
  51. Hajiahmadian M, Vajargah MF, Farsani HG, Chorchi MM (2012) Effect of Spirulina platensis meal as feed additive on growth performance and survival rate in golden barb fish, Punius gelius (Hamilton, 1822). J Fish Int 7:61–64Google Scholar
  52. Halim R, Danquah MK, Webley PA (2012) Extraction of oil from microalgae for biodiesel production: a review. Biotechnol Adv 30:709–732PubMedCrossRefGoogle Scholar
  53. Hannon M, Gimpel J, Tran M, Rasala B, Mayfield S (2010) Biofuels from algae: challenges and potential. Biofuels 1:763–784PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hemaiswarya S, Raja R, Kumar RR, Ganesan V, Anbazhagan C (2011) Microalgae: a sustainable feed source for aquaculture. World J Microb Biot 27:1737–1746CrossRefGoogle Scholar
  55. Horn MH, Messer KS (1992) Fish guts as a chemical reactor: a model of the alimentary canals of marine herbivorous. Mar Biol 113:527–535CrossRefGoogle Scholar
  56. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54:621–639PubMedCrossRefGoogle Scholar
  57. Hussein EES, Dabrowski K, El-Saidy DM, Lee BJ (2013) Enhancing the growth of Nile tilapia larvae/juveniles by replacing plant (gluten) protein with algae protein. Aquaculture Res 44:937–949CrossRefGoogle Scholar
  58. Ibrahem M, Mohamed MF, Ibrahim MA (2013) The role of Spirulina platensis (Arthrospira platensis) in growth and immunity of Nile tilapia (Oreochromis niloticus) and its resistance to bacterial infection. J Agr Sci 5:109–117Google Scholar
  59. Jia Z, Liu Y, Daroch M, Geng S, Cheng JJ (2014) Screening, growth medium optimisation and heterotrophic cultivation of microalgae for biodiesel production. Appl Biochem Biotech 173:1667–1679CrossRefGoogle Scholar
  60. Jo MJ, Hur SB (2015) Growth and nutritional composition of Eustigmatophyceae Monodus subterraneus and Nannochloropsis oceanica in autotrophic and mixotrophic culture. Ocean Polar Res 37:61–71CrossRefGoogle Scholar
  61. Ju ZY, Deng DF, Dominy W (2012) A defatted microalgae (Haematococcus pluvialis) meal as a protein ingredient to partially replace fishmeal in diets of Pacific white shrimp (Litopenaeus vannamei, Boone, 1931). Aquaculture 354:50–55CrossRefGoogle Scholar
  62. Kent M, Welladsen HM, Mangott A, Li Y (2015) Nutritional evaluation of Australian microalgae as potential human health supplements. PLoS One 10:e0118985PubMedPubMedCentralCrossRefGoogle Scholar
  63. Khatoon N, Pal R (2015) Microalgae in biotechnological application: a commercial approach. In: Bahadur B, Rajam MV, Sahijram L, Krishanamurthy MV (eds) Plant biology and biotechnology. Springer, New Delhi, pp 27–47CrossRefGoogle Scholar
  64. Kim SS, Rahimnejad S, Kim KW, Lee KJ (2013) Partial replacement of fishmeal with Spirulina pacifica in diets for parrot fish (Oplegnathus fasciatus). Turkish J Fish Aquat Sci 13:197–204Google Scholar
  65. Kiron V, Phromkunthong W, Huntley M, Archibald I, Scheemaker GD (2012) Marine microalgae from biorefinery as a potential feed protein source for Atlantic salmon, common carp and whiteleg shrimp. Aquaculture Nutr 18:521–531CrossRefGoogle Scholar
  66. Kiron V, Sørensen M, Huntley M, Vasanth GK, Gong Y, Dahle D, Palihawadana AM (2016) Defatted biomass of the microalga, Desmodesmus sp., can replace fishmeal in the feeds for Atlantic salmon. Front Mar Sci 3: 67Google Scholar
  67. Kitajima C (1983) Actual examples of mass cultures. In: Koseikaku K (ed) The rotifer Brachionus plicatilis—biology and mass culture. Japanese Fisheries Society, Tokyo, pp 102–128Google Scholar
  68. Kousoulaki K, Østbye TKK, Krasnov A, Torgersen JS, Mørkøre T, Sweetman J (2015) Metabolism, health and fillet nutritional quality in Atlantic salmon (Salmo salar) fed diets containing n-3-rich microalgae. J Nutr Sci 4:e24PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lang I, Hodac L, Friedl T, Feussner I (2011) Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biol 11:1–16CrossRefGoogle Scholar
  70. Li J, Liu Y, Cheng JJ, Mos M, Daroch M (2015) Biological potential of microalgae in China for biorefinery-based production of biofuels and high value compounds. New Biotech 32:588–596CrossRefGoogle Scholar
  71. Li MH, Robinson EH, Tucker CS, Manning BB, Khoo L (2009a) Effects of dried algae Schizochytrium sp., a rich source of docosahexaenoic acid, on growth, fatty acid composition, and sensory quality of channel catfish Ictalurus punctatus. Aquaculture 292:232–236CrossRefGoogle Scholar
  72. Li P, Mai K, Trushenski J, Wu G (2009b) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37:43–53PubMedCrossRefGoogle Scholar
  73. Li SS, Tsai HJ (2009) Transgenic microalgae as a non-antibiotic bactericide producer to defend against bacterial pathogen infection in the fish digestive tract. Fish Shellfish Immunol 26:316–325PubMedCrossRefGoogle Scholar
  74. Liao WL, Nur-E-Borhan SA, Okada S, Matsui T, Yamaguchi K (1993) Pigmentation of cultured black tiger prawn by feeding with a Spirulina-supplemented diet. Nippon Suisan Gakk 59:165–169CrossRefGoogle Scholar
  75. Liu Y, Tang J, Li J, Daroch M, Cheng JJ (2014) Efficient production of triacylglycerols rich in docosahexaenoic acid (DHA) by osmo-heterotrophic marine protists. Appl Microbiol Biotechnol 98:9643PubMedCrossRefGoogle Scholar
  76. Lu W, Alam MA, Pan Y, Wu J, Wang ZM, Yuan ZH (2016) A new approach of microalgal biomass pretreatment using deep eutectic solvents for enhanced lipid recovery for biodiesel production. Bioresour Technol 218:123–128PubMedCrossRefGoogle Scholar
  77. Madhumathi M, Rengasamy R (2011) Antioxidant status of Penaeus monodon fed with Dunaliella salina supplemented diet and resistance against WSSV. Int J Eng Sci Tech 3:7249–7259Google Scholar
  78. Maliwat GC, Velasquez S, Robil JL, Chan M, Traifalgar RF, Tayamen M, Ragaza JA (2017) Growth and immune response of giant freshwater prawn Macrobrachium rosenbergii (De Man) postlarvae fed diets containing Chlorella vulgaris (Beijerinck). Aquac Res 48:1666–1676CrossRefGoogle Scholar
  79. Matsuno TKM, Iwahashi M, Koike T, Okada M (1980) Intensification of color of red tilapia with lutein, rhodoxanthin and Spirulina. Bull Chem Soc Jap 46:479–482Google Scholar
  80. Matsuno TNS, Iwahashi M, Koike T, Okada M (1979) Intensification of color of fancy red carp with zeaxanthin and myxoxanthophyll, major carotenoid constituents of Spirulina. Bull Chem Soc Jap 45:627–632Google Scholar
  81. Medina-Félix D, López-Elías JA, Martínez-Córdova LR, López-Torres MA, Hernández-López J, Rivas-Vega ME, Mendoza-Cano F (2014) Evaluation of the productive and physiological responses of Litopenaeus vannamei infected with WSSV and fed diets enriched with Dunaliella sp. J Invertebr Pathol 117:9–12PubMedCrossRefGoogle Scholar
  82. Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177:272–280CrossRefGoogle Scholar
  83. Mendes A, Reis A, Vasconcelos R, Guerra P, Lopes da Silva T (2009) Crypthecodinium cohnii with emphasis on DHA production: a review. J Appl Phycol 21:199–214CrossRefGoogle Scholar
  84. Miki W, Yamaguchi K, Konosu S (1986) Carotenoid composition of Spirulina maxima. Nippon Suisan Gakk 52:1225–1227CrossRefGoogle Scholar
  85. Miller MR, Nichols PD, Carter CG (2007) Replacement of dietary fish oil for Atlantic salmon parr (Salmo salar L.) with a stearidonic acid containing oil has no effect on omega-3 long-chain polyunsaturated fatty acid concentrations. Comp Biochem Physiol B 146:197–206PubMedCrossRefGoogle Scholar
  86. Mori TMT, Miki W, Yamaguchi K, Konosu S, Watanabe T (1987) Pigmentation of cultured sweet smelt fed diets supplemented with a blue-green alga Spirulina maxima. Nippon Suisan Gakk 53:433–438CrossRefGoogle Scholar
  87. Mustafa MG, Nakagawa H (1995) A review: dietary benefits of algae as an additive in fish feed. Isr J Aquacult 47:155–162Google Scholar
  88. Namaei Kohal M, Esmaeili Fereidouni A, Firouzbakhsh F, Hayati I (2017) Effects of dietary incorporation of Arthrospira (Spirulina) platensis meal on growth, survival, body composition, and reproductive performance of red cherry shrimp Neocaridina davidi (Crustacea, Atyidae) over successive spawnings. J Appl Phycol. doi:10.1007/s10811-017-1220-5
  89. Nasopoulou C, Zabetakis I (2012) Benefits of fish oil replacement by plant originated oils in compounded fish feeds. A review. LWT-Food Sci Technol 47:217–224CrossRefGoogle Scholar
  90. Nath P, Khozin-Goldberg I, Cohen Z, Boussiba S, Zilberg D (2012) Dietary supplementation with the microalgae Parietochloris incisa increases survival and stress resistance in guppy (Poecilia reticulata) fry. Aquaculture Nutr 18:167–180CrossRefGoogle Scholar
  91. Norambuena F, Hermon K, Skrzypczyk V, Emery JA, Sharon Y, Beard A, Turchini GM (2015) Algae in fish feed: performances and fatty acid metabolism in juvenile Atlantic salmon. PLoS One 10:e0124042PubMedPubMedCentralCrossRefGoogle Scholar
  92. Origin Oil (2014) Origin Oil-White-Paper-Algae-As-Aquafeed (http://www.originclear.com/pdf/OriginOil-White-Paper-Algae-As-Aquafeed.pdf)
  93. Okada SLW, Mori T, Yamaguchi K, Watanabe T (1991) Pigmentation of cultured stripedjack reared on diets supplemented with the blue-green alga Spirulina maxima. Nippon Suisan Gakk 57:1403–1406CrossRefGoogle Scholar
  94. Olvera-Novoa MA, Dominguez-Cen LJ, Olivera-Castillo L, Martínez-Palacios CA (1998) Effect of the use of the microalgae Spirulina maxima as fishmeal replacement in diets for tilapia, Oreochromis mossambicus (Peters), fry. Aquac Res 29:709–715CrossRefGoogle Scholar
  95. Pacheco-Vega JM, Sánchez-Saavedra MP, Cadena-Roa MA, Tovar-Ramírez D (2016) Lipid digestibility and performance index of Litopenaeus vannamei fed with Chaetoceros muelleri cultured in two different enriched media. J Appl Phycol 28:2379–2385CrossRefGoogle Scholar
  96. Parisenti J, Beirão L, Maraschin M, Mourino J, Do Nascimento Vieira F, Bedin L, Rodrigues E (2011) Pigmentation and carotenoid content of shrimp fed with Haematococcus pluvialis and soy lecithin. Aquac Nutr 17:e530–e535CrossRefGoogle Scholar
  97. Patterson D, Delbert M, Gatlin DM (2013) Evaluation of whole and lipid-extracted algae meals in te diets of juvenile red drum (Sciaenops ocellatus). Aquaculture 416-417:92–98CrossRefGoogle Scholar
  98. Peng J, Yuan JP, Wang JH (2012) Effect of diets supplemented with different sources of astaxanthin on the gonad of the sea urchin Anthocidaris crassispina. Nutrients 4:922–934PubMedPubMedCentralCrossRefGoogle Scholar
  99. Pike IH, Jackson A (2010) Fish oil: production and use now and in the future. Lipid Technol 22:59–61CrossRefGoogle Scholar
  100. Priyadarshani I, Rath B (2012) Commercial and industrial application of microalgae—a review. J Algal Biomass Utiln 3:89–100Google Scholar
  101. Qiao H, Cong C, Sun C, Li B, Wang J, Zhang L (2016) Effect of culture conditions on growth, fatty acid composition and DHA/EPA ratio of Phaeodactylum tricornutum. Aquaculture 452:311–317CrossRefGoogle Scholar
  102. Qiao H, Wang H, Song Z, Ma J, Li B, Liu X, Zhang S, Wang J, Zhang L (2014) Effects of dietary fish oil replacement by microalgae raw materials on growth performance, body composition and fatty acid profile of juvenile olive flounder, Paralichthys olivaceus. Aquaculture Nutr 20:646–653CrossRefGoogle Scholar
  103. Reitan KI, Rainuzzo JR, Øie G, Olsen Y (1997) A review of the nutritional effects of algae in marine fish larvae. Aquaculture 155:207–221CrossRefGoogle Scholar
  104. Ren LJ, Ji XJ, Huang H, Qu L, Feng Y, Tong QQ, Ouyang PK (2010) Development of a stepwise aeration control strategy for efficient docosahexaenoic acid production by Schizochytrium sp. Appl Microbiol Biotechnol 87:1649–1656PubMedCrossRefGoogle Scholar
  105. Reyes-Becerril M, Guardiola F, Rojas M, Ascencio-Valle F, Esteban MÁ (2013) Dietary administration of microalgae Navicula sp. affects immune status and gene expression of gilthead seabream (Sparus aurata). Fish Shellfish Immunol 35:883–889PubMedCrossRefGoogle Scholar
  106. Ribeiro AR, Gonçalves A, Barbeiro M, Bandarra N, Nunes ML, Carvalho ML, Silva J, Navalho J, Dinis MT, Silva T, Dias J (2017) Phaeodactylum tricornutum in finishing diets for gilthead seabream: effects on skin pigmentation, sensory properties and nutritional value. J Appl Phycol 29:1945–1956CrossRefGoogle Scholar
  107. Rincón DD, Velásquez HA, Dávila MJ, Semprun AM, Morales ED, Hernández JL (2012) Substitution levels of fishmeal by Arthrospira (= Spirulina) maxima meal in experimental diets for red tilapia fingerlings (Oreochromis sp.). Rev Colomb Cienc Pec 25:430–437Google Scholar
  108. Roy SS, Pal R (2014) Microalgae in aquaculture: a review with special references to nutritional value and fish dietetics. Proc Zool Soc 68:1–8CrossRefGoogle Scholar
  109. Ruangsomboon S, Choochote S, Taveekijakarn P (2010) Growth performance and nutritional composition of red tilapia (Oreochromis niloticus x O. mossambicus) fed diets containing raw Spirulina platensis. The International Conference on Sustainable Community Development 2010. 21–23 January 2010. Khon Kaen University, Nongkhai Campus, Thailand and Vientiane, Lao PDRGoogle Scholar
  110. Ryan AS, Zeller S, Nelson EB (2010) Safety evaluation of single cell oils and the regulatory requirements for use as a food ingredient. In: Cohen Z, Ratledge C (eds) Single cell oils: microbial and algal oils. AOCS Publishing, Urbana, pp 317–350CrossRefGoogle Scholar
  111. Ryckebosch E, Bruneel C, Termote-Verhalle R, Goiris K, Muylaert K, Foubert I (2014) Nutritional evaluation of microalgae oils rich in omega-3 long chain polyunsaturated fatty acids as an alternative for fish oil. Food Chem 160:393–400PubMedCrossRefGoogle Scholar
  112. Sarker P, Gamble M, Kelson S, Kapuscinski A (2016a) Nile tilapia (Oreochromis niloticus) show high digestibility of lipid and fatty acids from marine Schizochytrium sp. and of protein and essential amino acids from freshwater Spirulina sp. feed ingredients. Aquac Nutr 22:109–119CrossRefGoogle Scholar
  113. Sarker PK, Kapuscinski AR, Lanois AJ, Livesey ED, Bernhard KP, Coley ML (2016b) Towards sustainable aquafeeds: complete substitution of fish oil with marine microalga Schizochytrium sp. improves growth and fatty acid deposition in juvenile Nile tilapia (Oreochromis niloticus). PloS One 11:e0156684PubMedPubMedCentralCrossRefGoogle Scholar
  114. Shah MMR, Liang Y, Cheng JJ, Daroch M (2016) Astaxanthin-producing green microalga Haematococcus pluvialis: from single cell to high value commercial products. Front Plant Sci 7:531PubMedPubMedCentralGoogle Scholar
  115. Sharma K, Schenk PM (2015) Rapid induction of omega-3 fatty acids (EPA) in Nannochloropsis sp. by UV- C radiation. Biotechnol Bioeng 112:1243–1249PubMedCrossRefGoogle Scholar
  116. Sharma SM, Panta K (2012) Use of Spirulina cultured in industrial effluents as a feed supplement on Sarotherodon mossambicus. Sonsik J 4:39–44Google Scholar
  117. Shields RJ, Lupatsch I (2012) Algae for aquaculture and animal feeds. Anim Sci 21:23–37Google Scholar
  118. Skrede A, Mydland L, Ahlstrøm Ø, Reitan K, Gislerød H, Øverland M (2011) Evaluation of microalgae as sources of digestible nutrients for monogastric animals. J Anim Feed Sci 20:131–142CrossRefGoogle Scholar
  119. Sommer TR, D'Souza FML, Morrissy NM (1992) Pigmentation of adult rainbow trout, Oncorhynchus mykiss, using the green alga Haematococcus pluvialis. Aquaculture 106:63–74CrossRefGoogle Scholar
  120. Sommer TR, Potts WT, Morrissy NM (1991) Utilization of microalgal astaxanthin by rainbow trout (Oncorhynchus mykiss). Aquaculture 94:79–88CrossRefGoogle Scholar
  121. Sørensen I, Rose JK, Doyle JJ, Domozych DS, Willats WG (2012) The Charophycean green algae as model systems to study plant cell walls and other evolutionary adaptations that gave rise to land plants. Plant Signal Behav 7:1–3PubMedPubMedCentralCrossRefGoogle Scholar
  122. Sørensen M, Berge GM, Reitan KI, Ruyter B (2016) Microalga Phaeodactylum tricornutum in feed for Atlantic salmon (Salmo salar)—effect on nutrient digestibility, growth and utilization of feed. Aquaculture 460:116–123CrossRefGoogle Scholar
  123. Sprague M, Dick JR, Tocher DR (2016) Impact of sustainable feeds on omega-3 long-chain fatty acid levels in farmed Atlantic salmon, 2006–2015. Sci Rep 6:21892PubMedPubMedCentralCrossRefGoogle Scholar
  124. Suhnel S (2008) Utilizaçao de diferentes dietas em reprodutores davieira Nodipecten nodosus (L.) em laboratorio e seu efeito na maturaçao, no rendimento larval e na produçao de pre-sementes. PhD thesis, Universidade Federal de Santa Catarina, 155pGoogle Scholar
  125. Sydney EB, Sturm W, de Carvalho JC, Thomaz-Soccol V, Larroche C, Pandey A, Soccol CR (2010) Potential carbon dioxide fixation by industrially important microalgae. Bioresour Technol 101:5892–5896PubMedCrossRefGoogle Scholar
  126. Tacon AGJ, Metian M (2015) Feed matters: satisfying the feed demand of aquaculture. Rev. Fish Sci Aqua 23:1–10CrossRefGoogle Scholar
  127. Teimouri M, Amirkolaie AK, Yeganeh S (2013) The effects of dietary supplement of Spirulina platensis on blood carotenoid concentration and fillet color stability in rainbow trout (Oncorhynchus mykiss). Aquaculture 415:224–228CrossRefGoogle Scholar
  128. Thompson GA (1996) Lipids and membrane function in green algae. Lipids Lipid Metab 1302:17–45CrossRefGoogle Scholar
  129. Tibaldi E, Zittelli GC, Parisi G, Bruno M, Giorgi G, Tulli F, Venturini S, Tredici M, Poli B (2015) Growth performance and quality traits of European sea bass (D. labrax) fed diets including increasing levels of freeze-dried Isochrysis sp.(T-ISO) biomass as a source of protein and n-3 long chain PUFA in partial substitution of fish derivatives. Aquaculture 440:60–68CrossRefGoogle Scholar
  130. Tibbetts SM, Bjornsson WJ, McGinn PJ (2015a) Biochemical composition and amino acid profiles of Nannochloropsis granulata algal biomass before and after supercritical fluid CO2 extraction at two processing temperatures. Animal Feed Sci Technol 204:62–71CrossRefGoogle Scholar
  131. Tibbetts SM, Melanson RJ, Park KC, Banskota AH, Stefanova R, McGinn PJ (2015b) Nutritional evaluation of whole and lipid-extracted biomass of the microalga Scenedesmus sp. AMDD isolated in Saskatchewan, Canada for animal feeds: proximate, amino acid, fatty acid, carotenoid and elemental composition. Current Biotech 4:530–546CrossRefGoogle Scholar
  132. Tibbetts SM, Milley JE, Lall SP (2006) Apparent protein and energy digestibility of common and alternative feed ingredients by Atlantic cod, Gadus morhua (Linnaeus, 1758). Aquaculture 261:1314–1327CrossRefGoogle Scholar
  133. Tibbetts SM, Milley JE, Lall SP (2015c) Chemical composition and nutritional properties of freshwater and marine microalgal biomass cultured in photobioreactors. J Appl Phycol 27:1109–1119CrossRefGoogle Scholar
  134. Tibbetts SM, Whitney CG, MacPherson MJ, Bhatti S, Banskota AH, Stefanova R, McGinn PJ (2015d) Biochemical characterization of microalgal biomass from freshwater species isolated in Alberta, Canada for animal feed applications. Algal Res 11:435–447CrossRefGoogle Scholar
  135. Lorenz RT, Cysewski GR (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167Google Scholar
  136. Tulli F, Chini Zittelli G, Giorgi G, Poli BM, Tibaldi E, Tredici MR (2012) Effect of the inclusion of dried Tetraselmis suecica on growth, feed utilization, and fillet composition of european sea bass juveniles fed organic diets. J Aquat Food Prod T 21:188–197CrossRefGoogle Scholar
  137. Turchini GM, Torstensen BE, Ng WK (2009) Fish oil replacement in finfish nutrition. Rev Aquacult 1:10–57CrossRefGoogle Scholar
  138. Velasquez SF, Chan MA, Abisado RG, Traifalgar RFM, Tayamen MM, Maliwat GCF, Ragaza JA (2016) Dietary Spirulina (Arthrospira platensis) replacement enhances performance of juvenile Nile tilapia (Oreochromis niloticus). J Appl Phycol 28:1023–1030CrossRefGoogle Scholar
  139. Vizcaíno A, López G, Sáez M, Jiménez J, Barros A, Hidalgo L, Camacho-Rodríguez J, Martínez T, Cerón-García M, Alarcón F (2014) Effects of the microalga Scenedesmus almeriensis as fishmeal alternative in diets for gilthead sea bream, Sparus aurata, juveniles. Aquaculture 431:34–43CrossRefGoogle Scholar
  140. Vizcaíno AJ, Saéz MI, López G, Arizcun M, Abellán E, Martínez TF, Cerón-García MC, Alarcón FJ (2016) Tetraselmis suecia and Tisochrysis lutea meal as dietary ingredients for gilthead sea bream (Sparus aurata L.) fry. J Appl Phycol 28:2843–2855CrossRefGoogle Scholar
  141. Walker AB, Berlinsky DL (2011) Effects of partial replacement of fishmeal protein by microalgae on growth, feed intake, and body composition of Atlantic cod. N Am J Aquacult 73:76–83Google Scholar
  142. Walker DA (2009) Biofuels, facts, fantasy, and feasibility. J Appl Phycol 21:509–517CrossRefGoogle Scholar
  143. Wan C, Alam MA, Zhao XQ, Zhang XY, Guo SL, Ho SH, Chang JS, Bai FW (2015) Current progress and future prospect of microalgal biomass harvest using various flocculation technologies. Bioresour Technol 184:251–257PubMedCrossRefGoogle Scholar
  144. Wang Y, Li M, Filer K, Xue Y, Ai Q, Mai K (2016) Evaluation of Schizochytrium meal in microdiets of Pacific white shrimp (Litopenaeus vannamei) larvae. Aquac Res:1–9. doi:10.1111/are.13068
  145. Watanabe T, Liao W, Takeuchi T, Yamamoto H (1990) Effect of dietary Spirulina supplement on growth performance and flesh lipids of cultured striped jack. J Tokyo Univ Fish 77:231–239Google Scholar
  146. Watanuki H, Ota K, Tassakka AR, Sakai M, Kato T, Sakai M (2006) Immunostimulant effects of dietary Spirulina platensis on carp, Cyprinus carpio. Aquaculture 258:157–163CrossRefGoogle Scholar
  147. White RL, Ryan RA (2015) Long-term cultivation of algae in open-raceway ponds: essons from the field. Ind Biotechnol 11:213–220CrossRefGoogle Scholar
  148. Xiangjun S, Chang Y, Ye Y, Ma Z, Liang Y, Li T, Jiang N, Xing W, Luo L (2012) The effect of dietary pigments on the coloration of Japanese ornamental carp (koi, Cyprinus carpio L.) Aquac Nutr 342–343:62–68Google Scholar
  149. Xu W, Gao Z, Qi Z, Qiu M, Peng JQ, Shao R (2014) Effect of dietary Chlorella on the growth performance and physiological parameters of gibel carp, Carassius auratus gibelio. Turkish J FishAquat Sci 14:53–57Google Scholar
  150. Yaakob Z, Ali E, Zainal A, Mohamad M, Takriff MS (2014) An overview: biomolecules from microalgae for animal feed and aquaculture. J Biol Res Thessalon 21:6PubMedPubMedCentralCrossRefGoogle Scholar
  151. Yeganeh S, Teimouri M, Amirkolaie AK (2015) Dietary effects of Spirulina platensis on hematological and serum biochemical parameters of rainbow trout (Oncorhynchus mykiss). Res Vet Sci 101:84–88PubMedCrossRefGoogle Scholar
  152. Zhang CN, Li XF, Xu WN, Jiang GZ, Lu KL, Wang LN, Liu WB (2013) Combined effects of dietary fructooligosaccharide and Bacillus licheniformis on innate immunity, antioxidant capability and disease resistance of triangular bream (Megalobrama terminalis). Fish Shellfish Immunol 35:1380–1386PubMedCrossRefGoogle Scholar
  153. Zhang Q, Qiu M, Xu W, Gao Z, Shao R, Qi Z (2014) Effects of dietary administration of Chlorella on the immune status of gibel carp, Carassius auratus gibelio. Ital J Anim Sci 13:3168CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.School of Environment and Energy, Shenzhen Graduate SchoolPeking UniversityShenzhenChina
  2. 2.Manatee Holdings Ltd.CourtenayCanada
  3. 3.Biosystem and Agricultural Engineering Department, Food and Agricultural Product CenterOklahoma State UniversityStillwaterUSA
  4. 4.CAS Key Laboratory of Renewable Energy, Chinese Academy of SciencesGuangzhou Institute of Energy ConversionGuangzhouChina
  5. 5.Environmental Studies Program, Dartmouth CollegeHanoverUSA
  6. 6.JEFO Nutrition Inc.QuebecCanada
  7. 7.Tecnologico de Monterrey, Campus MonterreyMonterreyMexico

Personalised recommendations