Skip to main content

Advertisement

SpringerLink
Log in

Microalgae in aquafeeds for a sustainable aquaculture industry

  • 4th AOAIS-Wuhan
  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • 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 289:38–45

    Article  CAS  PubMed  Google Scholar 

  • 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 186:293–310

    Article  Google Scholar 

  • Ambati RR, Phang SM, Ravi S, Aswathanarayana RG (2014) Astaxanthin: sources, extraction, stability, biological activities and its commercial applications—a review. Mar Drugs 12:128–152

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Atack T, Jauncey K, Matty A (1979) The utilization of some single cell proteins by fingerling mirror carp (Cyprinus carpio). Aquaculture 18:337–348

    Article  Google Scholar 

  • 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 270:178–185

    Article  CAS  Google Scholar 

  • 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 801–810

    Google Scholar 

  • 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 27:314–322

    Article  Google Scholar 

  • 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 27:857–863

    Article  CAS  Google Scholar 

  • Becker E (2007) Micro-algae as a source of protein. Biotechnol Adv 25:207–210

    Article  CAS  PubMed  Google Scholar 

  • Becker EW (1994) Microalgae: biotechnology and microbiology. Cambridge University Press, Cambridge, 293p

    Google Scholar 

  • 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 312–351

    Google Scholar 

  • Benemann J (2013). Microalgae for biofules and animal feeds. Energies 6:5869–5886

  • 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 19:110–121

    Article  CAS  Google Scholar 

  • 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 60:497–503

    Article  CAS  PubMed  Google Scholar 

  • Blazencic J (2007) Sistematika algi. NNK Internacional, Beograd

    Google Scholar 

  • 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):182–190

    Article  CAS  Google Scholar 

  • Borowitzka MA (2013a) High-value products from microalgae-their development and commercialisation. J Appl Phycol 25:743–756

    Article  CAS  Google Scholar 

  • Borowitzka MA (2013b) Dunaliella: biology, production, and markets. In: Richmond A, Hu Q (eds) Handbook of microalgal culture. John Wiley & Sons, Ltd, pp 359–368

    Chapter  Google Scholar 

  • Bowen SH (1976). Feeding ecology of the cichlid fish Sarotherodon mossambicus in Lake Sibaya, KwaZulu. Doctoral dissertation, Rhodes University, Grahamstown, South Africa

  • Brown M, Jeffrey S, Volkman J, Dunstan G (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151:315–331

    Article  CAS  Google Scholar 

  • 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 281–292

    Google Scholar 

  • 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 161:91–113

    Article  CAS  Google Scholar 

  • 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 334:110–116

    Article  CAS  Google Scholar 

  • Carter CG, Bransden MP, Lewis TE, Nichols PD (2003) Potential of Thraustochytrids to partially replace fish oil in Atlantic salmon feeds. Mar Biotechnol 5:480–492

    Article  CAS  PubMed  Google Scholar 

  • 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 32:719–723

    Article  Google Scholar 

  • 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 38:1729–1739

    Article  CAS  PubMed  Google Scholar 

  • 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 147:569–576

    Article  CAS  PubMed  Google Scholar 

  • 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 36:1517–1525

    Article  CAS  Google Scholar 

  • 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 436:95–103

    Article  CAS  Google Scholar 

  • 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 191:407–413

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Chi Z, O’Fallon JV, Zheng Y, Chakraborty M, Laskar DD (2010) System integration for producing microalgae as biofuel feedstock. Biofuels 1:889–910

    Article  CAS  Google Scholar 

  • 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 98:1433–1439

    Article  CAS  PubMed  Google Scholar 

  • 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 146:192–199

    Article  CAS  PubMed  Google Scholar 

  • Das BK, Pradhan J, Sahu S (2009) The effect of Euglena viridis on immune response of rohu, Labeo rohita (Ham.) Fish Shellfish Immunol 26:871–876

    Article  CAS  PubMed  Google Scholar 

  • Davis R, Aden A, Pienkos PT (2011) Techno-economic analysis of autotrophic microalgae for fuel production. Appl Energ 88:3524–3531

    Article  Google Scholar 

  • 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 34:277–289

    Article  Google Scholar 

  • 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 51:83–86

    Article  Google Scholar 

  • El-Sayed AFM (1994) Evaluation of soybean meal, Spirulina meal and chicken offal meal as protein sources for silver seabream (Rhabdosargus sarba) fingerlings. Aquaculture 127:169–176

    Article  CAS  Google Scholar 

  • 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. 82p

  • 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

  • FAO (2007) The state of world fisheries and aquaculture. FAO, Rome. (http://www.fao.org/docrep/fao/009/a0699e/a0699e.pdf )

  • FAO (2012) The state of world fisheries and aquaculture. FAO, Rome. (http://www.fao.org/docrep/016/i2727e/i2727e.pdf)

  • FAO (2014) The state of world fisheries and aquaculture: opportunities and challenges. FAO, Rome. (http://www.fao.org/3/a-i3720e.pdf )

  • 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 )

  • FDA (2010) http://www.fda.gov/regulatoryinformation/legislation/federal food drug and cosmetic act fdcact/default. html)

  • 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 277:109–116

    Article  CAS  Google Scholar 

  • 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

  • Guedes AC, Malcata FX (2012) Nutritional value and uses of microalgae in aquaculture. In: Muchlisin Z (ed) Aquaculture. INTECH, Riejeka, pp 59–78

    Google Scholar 

  • Guschina IA, Harwood JL (2013) Algal lipids and their metabolism. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy. Springer, Dordrecht, pp 17–36

    Chapter  Google Scholar 

  • 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: 1011

  • 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 7:61–64

    Google Scholar 

  • Halim R, Danquah MK, Webley PA (2012) Extraction of oil from microalgae for biodiesel production: a review. Biotechnol Adv 30:709–732

    Article  CAS  PubMed  Google Scholar 

  • Hannon M, Gimpel J, Tran M, Rasala B, Mayfield S (2010) Biofuels from algae: challenges and potential. Biofuels 1:763–784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hemaiswarya S, Raja R, Kumar RR, Ganesan V, Anbazhagan C (2011) Microalgae: a sustainable feed source for aquaculture. World J Microb Biot 27:1737–1746

    Article  Google Scholar 

  • Horn MH, Messer KS (1992) Fish guts as a chemical reactor: a model of the alimentary canals of marine herbivorous. Mar Biol 113:527–535

    Article  Google Scholar 

  • 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 54:621–639

    Article  CAS  PubMed  Google Scholar 

  • 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 44:937–949

    Article  CAS  Google Scholar 

  • 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 5:109–117

    Google Scholar 

  • IFFO (2016) Fishmeal and fish oil statistical yearbook http://www.seafish.org/media/publications/SeafishFishmealandFishOilFactsandFigures_201612.pdf

  • 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 173:1667–1679

    Article  CAS  Google Scholar 

  • Jo MJ, Hur SB (2015) Growth and nutritional composition of Eustigmatophyceae Monodus subterraneus and Nannochloropsis oceanica in autotrophic and mixotrophic culture. Ocean Polar Res 37:61–71

    Article  CAS  Google Scholar 

  • 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 354:50–55

    Article  CAS  Google Scholar 

  • Kent M, Welladsen HM, Mangott A, Li Y (2015) Nutritional evaluation of Australian microalgae as potential human health supplements. PLoS One 10:e0118985

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 27–47

    Chapter  Google Scholar 

  • 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 13:197–204

    Google Scholar 

  • 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 18:521–531

    Article  CAS  Google Scholar 

  • 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: 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 102–128

    Google Scholar 

  • 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:e24

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 11:1–16

    Article  CAS  Google Scholar 

  • 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 32:588–596

    Article  CAS  Google Scholar 

  • 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 292:232–236

    Article  CAS  Google Scholar 

  • Li P, Mai K, Trushenski J, Wu G (2009b) New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds. Amino Acids 37:43–53

    Article  PubMed  CAS  Google Scholar 

  • 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 26:316–325

    Article  PubMed  CAS  Google Scholar 

  • 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 59:165–169

    Article  CAS  Google Scholar 

  • 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 98:9643

    Article  CAS  PubMed  Google Scholar 

  • 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 218:123–128

    Article  CAS  PubMed  Google Scholar 

  • 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 3:7249–7259

    Google Scholar 

  • 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 48:1666–1676

    Article  CAS  Google Scholar 

  • Matsuno TKM, Iwahashi M, Koike T, Okada M (1980) Intensification of color of red tilapia with lutein, rhodoxanthin and Spirulina. Bull Chem Soc Jap 46:479–482

    CAS  Google Scholar 

  • 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 45:627–632

    CAS  Google Scholar 

  • 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 117:9–12

    Article  PubMed  Google Scholar 

  • Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177:272–280

    Article  CAS  Google Scholar 

  • 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 21:199–214

    Article  Google Scholar 

  • Miki W, Yamaguchi K, Konosu S (1986) Carotenoid composition of Spirulina maxima. Nippon Suisan Gakk 52:1225–1227

    Article  CAS  Google Scholar 

  • 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 146:197–206

    Article  PubMed  CAS  Google Scholar 

  • 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 53:433–438

    Article  CAS  Google Scholar 

  • Mustafa MG, Nakagawa H (1995) A review: dietary benefits of algae as an additive in fish feed. Isr J Aquacult 47:155–162

  • 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

  • Nasopoulou C, Zabetakis I (2012) Benefits of fish oil replacement by plant originated oils in compounded fish feeds. A review. LWT-Food Sci Technol 47:217–224

    Article  CAS  Google Scholar 

  • 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 18:167–180

    Article  CAS  Google Scholar 

  • 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:e0124042

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Origin Oil (2014) Origin Oil-White-Paper-Algae-As-Aquafeed (http://www.originclear.com/pdf/OriginOil-White-Paper-Algae-As-Aquafeed.pdf)

  • 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 57:1403–1406

    Article  Google Scholar 

  • 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 29:709–715

    Article  Google Scholar 

  • 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 28:2379–2385

    Article  CAS  Google Scholar 

  • 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–e535

    Article  Google Scholar 

  • 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 416-417:92–98

    Article  CAS  Google Scholar 

  • 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 4:922–934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pike IH, Jackson A (2010) Fish oil: production and use now and in the future. Lipid Technol 22:59–61

    Article  CAS  Google Scholar 

  • Priyadarshani I, Rath B (2012) Commercial and industrial application of microalgae—a review. J Algal Biomass Utiln 3:89–100

    Google Scholar 

  • 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 452:311–317

    Article  CAS  Google Scholar 

  • 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 20:646–653

    Article  CAS  Google Scholar 

  • Reitan KI, Rainuzzo JR, Øie G, Olsen Y (1997) A review of the nutritional effects of algae in marine fish larvae. Aquaculture 155:207–221

    Article  Google Scholar 

  • 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 87:1649–1656

    Article  CAS  PubMed  Google Scholar 

  • 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 35:883–889

    Article  CAS  PubMed  Google Scholar 

  • 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 29:1945–1956

    Article  CAS  Google Scholar 

  • 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 25:430–437

    Google Scholar 

  • Roy SS, Pal R (2014) Microalgae in aquaculture: a review with special references to nutritional value and fish dietetics. Proc Zool Soc 68:1–8

    Article  CAS  Google Scholar 

  • 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 PDR

  • 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 317–350

    Chapter  Google Scholar 

  • 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 160:393–400

    Article  CAS  PubMed  Google Scholar 

  • 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 22:109–119

    Article  CAS  Google Scholar 

  • 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:e0156684

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 7:531

    PubMed  PubMed Central  Google Scholar 

  • Sharma K, Schenk PM (2015) Rapid induction of omega-3 fatty acids (EPA) in Nannochloropsis sp. by UV- C radiation. Biotechnol Bioeng 112:1243–1249

    Article  CAS  PubMed  Google Scholar 

  • Sharma SM, Panta K (2012) Use of Spirulina cultured in industrial effluents as a feed supplement on Sarotherodon mossambicus. Sonsik J 4:39–44

    CAS  Google Scholar 

  • Shields RJ, Lupatsch I (2012) Algae for aquaculture and animal feeds. Anim Sci 21:23–37

    Google Scholar 

  • 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 20:131–142

    Article  Google Scholar 

  • Sommer TR, D'Souza FML, Morrissy NM (1992) Pigmentation of adult rainbow trout, Oncorhynchus mykiss, using the green alga Haematococcus pluvialis. Aquaculture 106:63–74

    Article  Google Scholar 

  • Sommer TR, Potts WT, Morrissy NM (1991) Utilization of microalgal astaxanthin by rainbow trout (Oncorhynchus mykiss). Aquaculture 94:79–88

    Article  CAS  Google Scholar 

  • 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 7:1–3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 460:116–123

    Article  CAS  Google Scholar 

  • 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 6:21892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 155p

  • 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 101:5892–5896

    Article  CAS  PubMed  Google Scholar 

  • Tacon AGJ, Metian M (2015) Feed matters: satisfying the feed demand of aquaculture. Rev. Fish Sci Aqua 23:1–10

    Article  Google Scholar 

  • 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 415:224–228

    Article  CAS  Google Scholar 

  • Thompson GA (1996) Lipids and membrane function in green algae. Lipids Lipid Metab 1302:17–45

    Article  Google Scholar 

  • 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 440:60–68

    Article  CAS  Google Scholar 

  • 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 204:62–71

    Article  CAS  Google Scholar 

  • 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 4:530–546

    Article  CAS  Google Scholar 

  • 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 261:1314–1327

    Article  Google Scholar 

  • Tibbetts SM, Milley JE, Lall SP (2015c) Chemical composition and nutritional properties of freshwater and marine microalgal biomass cultured in photobioreactors. J Appl Phycol 27:1109–1119

    Article  CAS  Google Scholar 

  • 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 11:435–447

    Article  Google Scholar 

  • Lorenz RT, Cysewski GR (2000) Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. Trends Biotechnol 18:160–167

  • 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 21:188–197

    Article  Google Scholar 

  • Turchini GM, Torstensen BE, Ng WK (2009) Fish oil replacement in finfish nutrition. Rev Aquacult 1:10–57

    Article  Google Scholar 

  • 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 28:1023–1030

    Article  CAS  Google Scholar 

  • 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 431:34–43

    Article  CAS  Google Scholar 

  • 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 28:2843–2855

    Article  CAS  Google Scholar 

  • 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 73:76–83

    Google Scholar 

  • Walker DA (2009) Biofuels, facts, fantasy, and feasibility. J Appl Phycol 21:509–517

    Article  Google Scholar 

  • 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 184:251–257

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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 77:231–239

    Google Scholar 

  • Watanuki H, Ota K, Tassakka AR, Sakai M, Kato T, Sakai M (2006) Immunostimulant effects of dietary Spirulina platensis on carp, Cyprinus carpio. Aquaculture 258:157–163

    Article  Google Scholar 

  • White RL, Ryan RA (2015) Long-term cultivation of algae in open-raceway ponds: essons from the field. Ind Biotechnol 11:213–220

    Article  Google Scholar 

  • 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 342–343:62–68

    Google Scholar 

  • 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 14:53–57

    Google Scholar 

  • 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 21:6

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 101:84–88

    Article  PubMed  Google Scholar 

  • 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 35:1380–1386

    Article  CAS  PubMed  Google Scholar 

  • 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 13:3168

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to acknowledge the support of the National Natural Science Foundation of China for Young International Scientists Grant No. 31550110497), Shenzhen Municipal Government for Special Innovation Fund for Shenzhen Overseas High-level Personnel KQCX20140521150255300, Shenzhen Knowledge and Innovation Basic Research Grant JCYJ20160122151433832, and State Ocean Administration Grant 201305022.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Author notes

  1. Mahfuzur Rahman Shah MD.

    Present address: Manatee Holdings Ltd., 4097 Gartley Point Road, Courtenay, BC, V9N9T2, Canada

Authors and Affiliations

  1. School of Environment and Energy, Shenzhen Graduate School, Peking University, Shenzhen, 518055, China

    Mahfuzur Rahman Shah MD., Yuanmei Liang & Maurycy Daroch

  2. Biosystem and Agricultural Engineering Department, Food and Agricultural Product Center, Oklahoma State University, Room 104, Stillwater, OK, 74075, USA

    Giovanni Antonio Lutzu

  3. CAS Key Laboratory of Renewable Energy, Chinese Academy of Sciences, Guangzhou Institute of Energy Conversion, Guangzhou, 510640, China

    Asraful Alam MD.

  4. Environmental Studies Program, Dartmouth College, Hanover, NH, 03755, USA

    Pallab Sarker

  5. JEFO Nutrition Inc., 80 rue JEFO, Saint-Hyacinthe, Quebec, J2S 7B6, Canada

    M. A. Kabir Chowdhury

  6. Tecnologico de Monterrey, Campus Monterrey, Ave. Eugenio Garza Sada 2501, 64849, Monterrey, NL, Mexico

    Ali Parsaeimehr

Authors
  1. Mahfuzur Rahman Shah MD.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giovanni Antonio Lutzu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Asraful Alam MD.
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pallab Sarker
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. A. Kabir Chowdhury
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ali Parsaeimehr
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuanmei Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maurycy Daroch
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MS collected data, participated in preparation of the manuscript draft, and participated in assembly and editing of the final manuscript; GAL, MAA, AP, and YML collected data and participated in the preparation of the manuscript draft; PKS and KC participated in assembly and editing of the final manuscript; MD participated in the preparation of the manuscript draft and participated in the assembly and editing of the final manuscript.

Corresponding author

Correspondence to Maurycy Daroch.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shah, M.R., Lutzu, G.A., Alam, A. et al. Microalgae in aquafeeds for a sustainable aquaculture industry. J Appl Phycol 30, 197–213 (2018). https://doi.org/10.1007/s10811-017-1234-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1234-z

Keywords

Search

Navigation