Abstract
Fishmeal is an indispensable ingredient for most aquatic animals. However, the finite supply and escalating price of fishmeal seriously limit its use in aquaculture. Thus the development of new, sustainable protein ingredients has been a research focus. Microalgae are potential fishmeal alternatives owing to their high protein content and balanced amino acid profile. Studies suggest that suitable replacement of fishmeal with microalgae is beneficial for fish growth performance, but excessive replacement would induce poor growth and feed utilization. Therefore, this paper aims to review research on the maximum substitutional level of fishmeal by microalgae and propose the main issues and possible solutions for fishmeal replacement by microalgae. The maximum replacement level is affected by microalgal species, fish feeding habits, quality of fishmeal and microalgal meals, and supplemental levels of fishmeal in the control group. Microalgae could generally replace 100%, 95%, 95%, 64.1%, 25.6%, and 18.6% fishmeal protein in diets of carp, shrimp, catfish, tilapia, marine fish, and salmon and trout, respectively. The main issues with fishmeal replacement using microalgae include low production and high production cost, poor digestibility, and anti-nutritional factors. Possible solutions to these problems are recommended in this paper. Overall, microalgae are promising fishmeal alternatives in aquaculture.
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Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Abbott JK, Willard D, Xu J (2021) Feeding the dragon: The evolution of China’s fishery imports. Mar Policy 133:104733. https://doi.org/10.1016/j.marpol.2021.104733
Abdulrahman NM, Ameen HJH (2014) Replacement of fishmeal with microalgae Spirulina on common carp weight gain, meat and sensitive composition and survival. Pak J Nutr 13:93–98
Agboola JO, Teuling E, Wierenga PA, Gruppen H, Schrama JW (2019) Cell wall disruption: An effective strategy to improve the nutritive quality of microalgae in African catfish (Clarias gariepinus). Aquacult Nutr 25:783–797. https://doi.org/10.1111/anu.12896
Ahmad MT, Shariff M, Yusoff FMd, Goh YM, Banerjee S (2020) Applications of microalga Chlorella vulgaris in aquaculture. Rev Aquacult 12:328–346. https://doi.org/10.1111/raq.12320
Ahmad A, Hassan SW, Banat F (2022) An overview of microalgae biomass as a sustainable aquaculture feed ingredient: food security and circular economy. Bioengineered 13:9521–9547. https://doi.org/10.1080/21655979.2022.2061148
Akter T, Hossain A, Rabiul Islam M, Hossain MA, Das M, Rahman MM, Aye AT, Abdel-Tawwab M (2023) Effects of spirulina (Arthrospira platensis) as a fishmeal replacer in practical diets on growth performance, proximate composition, and amino acids profile of pabda catfish (Ompok pabda). J Appl Aquacult 35:69–82. https://doi.org/10.1080/10454438.2021.1936740
Alagawany M, Taha AE, Noreldin A, El-Tarabily KA, Abd El-Hack ME (2021) Nutritional applications of species of Spirulina and Chlorella in farmed fish: A review. Aquaculture 542:736841. https://doi.org/10.1016/j.aquaculture.2021.736841
Altmann BA, Rosenau S (2022) Spirulina as animal feed: opportunities and challenges. Foods 11:965. https://doi.org/10.3390/foods11070965
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
Barclay W, Apt K, Dong XD (2013) Commercial production of microalgae via fermentation. In: Richmond A, Hu Q (eds) Handbook of microalgal culture, 2nd edn. John Wiley & Sons, UK, pp 134–145
Becker W (2004a) Microalgae in human and animal nutrition. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell, Oxford, pp 312–351
Becker W (2004b) Microalgae for aquaculture. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell, Oxford, pp 352–364
Becker EW (2007) Micro-algae as a source of protein. Biotechnol Adv 25:207–210. https://doi.org/10.1016/j.biotechadv.2006.11.002
Benemann JR, Woertz I, Lundquist T (2018) Autotrophic microalgae biomass production: from niche markets to commodities. Ind Biotechnol 14:3–10. https://doi.org/10.1089/ind.2018.29118.jrb
Boyd CE, McNevin AA, Davis RP (2022) The contribution of fisheries and aquaculture to the global protein supply. Food Secur 14:805–827. https://doi.org/10.1007/s12571-021-01246-9
Brown MR, Jeffrey SW, Volkman JK, Dunstan GA (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151:315–331. https://doi.org/10.1016/S0044-8486(96)01501-3
Cao S-P, Zou T, Zhang P-Y, Han D, Jin J-Y, Liu H-K, Yang Y-X, Zhu X-M, Xie S-Q (2018a) Effects of dietary fishmeal replacement with Spirulina platensis on the growth, feed utilization, digestion and physiological parameters in juvenile gibel carp (Carassis auratus gibelio var. CAS III). Aquac Res 49:1320–1328. https://doi.org/10.1111/are.13590
Cao S, Zhang P, Zou T, Fei S, Han D, Jin J, Liu H, Yang Y, Zhu X, Xie S (2018b) Replacement of fishmeal by spirulina Arthrospira platensis affects growth, immune related-gene expression in gibel carp (Carassius auratus gibelio var. CAS III), and its challenge against Aeromonas hydrophila infection. Fish Shellfish Immun 79:265–273. https://doi.org/10.1016/j.fsi.2018.05.022
Cardinaletti G, Messina M, Bruno M, Tulli F, Poli BM, Giorgi G, Chini-Zittelli G, Tredici M, Tibaldi E (2018) Effects of graded levels of a blend of Tisochrysis lutea and Tetraselmis suecica dried biomass on growth and muscle tissue composition of European sea bass (Dicentrarchus labrax) fed diets low in fish meal and oil. Aquaculture 485:173–182. https://doi.org/10.1016/j.aquaculture.2017.11.049
Carneiro WF, Castro TFD, Orlando TM, Meurer F, Paula DAdJ, Virote BdCR, Vianna ARdCB, Murgas LDS (2020) Replacing fish meal by Chlorella sp. meal: Effects on zebrafish growth, reproductive performance, biochemical parameters and digestive enzymes. Aquaculture 528:735612. https://doi.org/10.1016/j.aquaculture.2020.735612
Chen F (1996) High cell density culture of microalgae in heterotrophic growth. Trends Biotechnol 14:421–426. https://doi.org/10.1016/0167-7799(96)10060-3
Chen W, Luo L, Han D, Long F, Chi Q, Hu Q (2021) Effect of dietary supplementation with Chlorella sorokiniana meal on the growth performance, antioxidant status, and immune response of rainbow trout (Oncorhynchus mykiss). J Appl Phycol 33:3113–3122. https://doi.org/10.1007/s10811-021-02541-w
Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306. https://doi.org/10.1016/j.biotechadv.2007.02.001
Córdova O, Passos F, Chamy R (2019) Enzymatic pretreatment of microalgae: cell wall disruption, biomass solubilisation and methane yield increase. Appl Biochem Biotechnol 189:787–797. https://doi.org/10.1007/s12010-019-03044-8
Craig S, Helfrich LA (2009) Understanding fish nutrition, feeds and feeding. Virginia Cooperative Extension (Publication 420-256). http://hdl.handle.net/10919/48950. Accessed 7 Apr 2014
de Farias Silva CE, Bertucco A (2016) Bioethanol from microalgae and cyanobacteria: A review and technological outlook. Process Biochem 51:1833–1842. https://doi.org/10.1016/j.procbio.2016.02.016
de la Higuera M, Garcia-Gallego M, Cardenete G, Suarez MD, Moyano FJ (1988) Evaluation of Lupin seed meal as an alternative protein source in feeding of rainbow trout (Salmo gairdneri). Aquaculture 71:37–50. https://doi.org/10.1016/0044-8486(88)90271-2
Dębowski M, Zieliński M, Kazimierowicz J, Kujawska N, Talbierz S (2020) Microalgae cultivation technologies as an opportunity for bioenergetic system development—advantages and limitations. Sustainability 12:9980. https://doi.org/10.3390/su12239980
Di Caprio F, Chelucci R, Francolini I, Altimari P, Pagnanelli F (2022) Extraction of microalgal starch and pigments by using different cell disruption methods and aqueous two-phase system. J Chem Technol Biotechnol 97:67–78. https://doi.org/10.1002/jctb.6910
Domozych DS, Serfis A, Kiemle SN, Gretz MR (2007) The structure and biochemistry of charophycean cell walls: I. Pectins of Penium margaritaceum. Protoplasma 230:99–115. https://doi.org/10.1007/s00709-006-0197-8
Domozych D, Ciancia M, Fangel J, Mikkelsen M, Ulvskov P, Willats W (2012) The cell walls of green algae: a journey through evolution and diversity. Front Plant Sci 3:82. https://doi.org/10.3389/fpls.2012.00082
El-fayoumy EA, Shanab S, Shalaby EA (2020) Metabolomics and biological activities of Chlorella vulgaris grown under modified growth medium (BG11) composition. CMU J Nat Sci 19:91–123. https://doi.org/10.12982/CMUJNS.2020.0007
El-Sayed A-FM (1994) Evaluation of soybean meal, spirulina meal and chicken offal meal as protein sources for silver seabream (Rhabdosargus sarba) fingerlings. Aquaculture 127:169–176. https://doi.org/10.1016/0044-8486(94)90423-5
El-Sheekh M, E-Shourbagy I, Shalaby S, Hosny S (2014) Effect of feeding Arthrospira platensis (Spirulina) on growth and carcass composition of hybrid red tilapia (Oreochromis niloticus x Oreochromis mossambicus). Turkish J Fish Aquat Sci 14:471–478. https://doi.org/10.4194/1303-2712-v14_2_18
European Commission (2021) Fishmeal and fish oil production and trade flows in the EU. Publication Office of the European Union, Luxembourg. https://op.europa.eu/en/publication-detail/-/publication/984cee38-475a-11ec-91ac-01aa75ed71a1/language-en
FAO (2020) The state of world fisheries and aquaculture 2020. Sustainability in action. Food and Agriculture Organization of the United Nations, Rome, Italy. https://www.fao.org/3/ca9229en/ca9229en.pdf
Foster M, Petrell R, Ito MR, Ward R (1995) Detection and counting of uneaten food pellets in a sea cage using image analysis. Aquacult Eng 14:251–269. https://doi.org/10.1016/0144-8609(94)00006-M
Francis G, Makkar HPS, Becker K (2001) Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture 199:197–227. https://doi.org/10.1016/s0044-8486(01)00526-9
Geldenhuys DJ, Walmsley RD, Toerien DF (1988) Quality of algal material produced on a fertilizer-tap water medium in outdoor plastic-enclosed systems. Aquaculture 68:157–164. https://doi.org/10.1016/0044-8486(88)90238-4
Gemede HF, Ratta N (2014) Antinutritional factors in plant foods: potential health benefits and adverse effects. Int J Nutr Food Sci 3:284–289. https://doi.org/10.11648/j.ijnfs.20140304.18
Glencross BD, Booth M, Allan GL (2007) A feed is only as good as its ingredients - a review of ingredient evaluation strategies for aquaculture feeds. Aquacult Nutr 13:17–34. https://doi.org/10.1111/j.1365-2095.2007.00450.x
Gong Y, Bandara T, Huntley M, Johnson ZI, Dias J, Dahle D, Sørensen M, Kiron V (2019) Microalgae Scenedesmus sp. as a potential ingredient in low fishmeal diets for Atlantic salmon (Salmo salar L.). Aquaculture 501:455–464. https://doi.org/10.1016/j.aquaculture.2018.11.049
Goswami RK, Mehariya S, Obulisamy PK, Verma P (2021) Advanced microalgae-based renewable biohydrogen production systems: A review. Bioresour Technol 320:124301. https://doi.org/10.1016/j.biortech.2020.124301
Grima EM, Acién Fernández FG, Robles Medina A (2013) Downstream processing of cell mass and products. In: Richmond A, Hu Q (eds) Handbook of microalgal culture, 2nd edn. John Wiley & Sons, UK, pp 267–309
Halim R, Danquah MK, Webley PA (2012) Extraction of oil from microalgae for biodiesel production: A review. Biotechnol Adv 30:709–732. https://doi.org/10.1016/j.biotechadv.2012.01.001
Hardy RW (2010) Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquac Res 41:770–776. https://doi.org/10.1111/j.1365-2109.2009.02349.x
Hemaiswarya S, Raja R, Kumar RR, Ganesan V, Anbazhagan C (2011) Microalgae: a sustainable feed source for aquaculture. World J Microbiol Biotechnol 27:1737–1746. https://doi.org/10.1007/s11274-010-0632-z
Hetta M, Mahmoud R, El-Senousy W, Ibrahim MK, El-Taweel G, Ali G (2014) Antiviral and antimicrobial activities of Spirulina platensis. World J Pharm Pharm Sci 3:31–39
Houston RD, Bean TP, Macqueen DJ, Gundappa MK, Jin YH, Jenkins TL, Selly SLC, Martin SAM, Stevens JR, Santos EM, Davie A, Robledo D (2020) Harnessing genomics to fast-track genetic improvement in aquaculture. Nat Rev Genet 21:389–409. https://doi.org/10.1038/s41576-020-0227-y
Hua K, Cobcroft JM, Cole A, Condon K, Jerry DR, Mangott A, Praeger C, Vucko MJ, Zeng C, Zenger K, Strugnell JM (2019) The future of aquatic protein: Implications for protein sources in aquaculture diets. One Earth 1:316–329. https://doi.org/10.1016/j.oneear.2019.10.018
Ibañez E, Cifuentes A (2013) Benefits of using algae as natural sources of functional ingredients. J Sci Food Agric 93:703–709. https://doi.org/10.1002/jsfa.6023
Ishaq AG, Matias-Peralta HM, Basri H (2016) Bioactive compounds from green microalga - Scenedesmus and its potential applications: a brief review. Pertanika J Trop Agric Sci 39:1–15
Jacob-Lopes E, Maroneze MM, Deprá MC, Sartori RB, Dias RR, Zepka LQ (2019) Bioactive food compounds from microalgae: an innovative framework on industrial biorefineries. Curr Opin Food Sci 25:1–7. https://doi.org/10.1016/j.cofs.2018.12.003
Jannathulla R, Rajaram V, Kalanjiam R, Ambasankar K, Muralidhar M, Dayal JS (2019) Fishmeal availability in the scenarios of climate change: Inevitability of fishmeal replacement in aquafeeds and approaches for the utilization of plant protein sources. Aquac Res 50:3493–3506. https://doi.org/10.1111/are.14324
Ju ZY, Deng D-F, 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 354–355:50–55. https://doi.org/10.1016/j.aquaculture.2012.04.028
Kamalam BS, Medale F, Panserat S (2017) Utilisation of dietary carbohydrates in farmed fishes: New insights on influencing factors, biological limitations and future strategies. Aquaculture 467:3–27. https://doi.org/10.1016/j.aquaculture.2016.02.007
Karapanagiotidis IT, Metsoviti MN, Gkalogianni EZ, Psofakis P, Asimaki A, Katsoulas N, Papapolymerou G, Zarkadas I (2022) The effects of replacing fishmeal by Chlorella vulgaris and fish oil by Schizochytrium sp. and Microchloropsis gaditana blend on growth performance, feed efficiency, muscle fatty acid composition and liver histology of gilthead seabream (Sparus aurata). Aquaculture 561:738709. https://doi.org/10.1016/j.aquaculture.2022.738709
Kavisri M, Marykutty A, Gopal P, Manickam E, Meivelu M (2021) Phytochemistry, bioactive potential and chemical characterization of metabolites from marine microalgae (Spirulina platensis) biomass. Biomass Convers Bior 13:1147–1154. https://doi.org/10.1007/s13399-021-01689-2
Kim S-S, Rahimnejad S, Kim K-W, Lee K-J (2013) Partial replacement of fish meal with Spirulina pacifica in diets for parrot fish (Oplegnathus fasciatus). Turkish J Fish Aquat Sci 13:197–204. https://doi.org/10.4194/1303-2712-v13_2_01
Kiron V, Phromkunthong W, Huntley M, Archibald I, De Scheemaker G (2012) Marine microalgae from biorefinery as a potential feed protein source for Atlantic salmon, common carp and whiteleg shrimp. Aquacult Nutr 18:521–531. https://doi.org/10.1111/j.1365-2095.2011.00923.x
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 Mari Sci 3:67. https://doi.org/10.3389/fmars.2016.00067
Knutsen HR, Ottesen OH, Palihawadana AM, Sandaa W, Sorensen M, Hagen O (2019) Muscle growth and changes in chemical composition of spotted wolffish juveniles (Anarhichas minor) fed diets with and without microalgae (Scenedesmus obliquus). Aquacult Rep 13:100175. https://doi.org/10.1016/j.aqrep.2018.11.001
Kotrbáček V, Doubek J, Doucha J (2015) The chlorococcalean alga Chlorella in animal nutrition: a review. J Appl Phycol 27:2173–2180. https://doi.org/10.1007/s10811-014-0516-y
Kovač DJ, Simeunović JB, Babić OB, Mišan AČ, Milovanović IL (2013) Algae in food and feed. Food Feed Res 40:21–31
Krogdahl Å, Bakke-McKellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquacult Nutr 9:361–371. https://doi.org/10.1046/j.1365-2095.2003.00264.x
Krogdahl Å, Hemre GI, Mommsen TP (2005) Carbohydrates in fish nutrition: digestion and absorption in postlarval stages. Aquacult Nutr 11:103–122. https://doi.org/10.1111/j.1365-2095.2004.00327.x
Lall SP (2022) The minerals. In: Hardy RW, Kaushik SJ (eds) Fish Nutrition, 4th edn. Academic Press, London, pp 469–554
Liu C, Liu H, Xu W, Han D, Xie S, Jin J, Yang Y, Zhu X (2019) Effects of dietary Arthrospira platensis supplementation on the growth, pigmentation, and antioxidation in yellow catfish (Pelteobagrus fulvidraco). Aquaculture 510:267–275. https://doi.org/10.1016/j.aquaculture.2019.05.067
Lupatsch I, Blake C (2013) Algae alternative: Chlorella studied as protein source in tilapia feeds. Glob Aquacult Advocate 16:78–79
Lürling M (2003) Phenotypic plasticity in the green algae Desmodesmus and Scenedesmus with special reference to the induction of defensive morphology. Ann Limnol-Int J Lim 39:85–101. https://doi.org/10.1051/limn/2003014
Maas RM, Verdegem MCJ, Wiegertjes GF, Schrama JW (2020) Carbohydrate utilisation by tilapia: a meta-analytical approach. Rev Aquacult 12:1851–1866. https://doi.org/10.1111/raq.12413
Macias-Sancho J, Poersch LH, Bauer W, Romano LA, Wasielesky W, Tesser MB (2014) Fishmeal substitution with Arthrospira (Spirulina platensis) in a practical diet for Litopenaeus vannamei: Effects on growth and immunological parameters. Aquaculture 426–427:120–125. https://doi.org/10.1016/j.aquaculture.2014.01.028
Maia JLd, Cardoso JS, Mastrantonio DJdS, Bierhals CK, Moreira JB, Costa JAV, Morais MGd (2020) Microalgae starch: A promising raw material for the bioethanol production. Int J Biol Macromol 165:2739–2749. https://doi.org/10.1016/j.ijbiomac.2020.10.159
Maisashvili A, Bryant H, Richardson J, Anderson D, Wickersham T, Drewery M (2015) The values of whole algae and lipid extracted algae meal for aquaculture. Algal Res 9:133–142. https://doi.org/10.1016/j.algal.2015.03.006
Markou G, Angelidaki I, Georgakakis D (2012) Microalgal carbohydrates: an overview of the factors influencing carbohydrates production, and of main bioconversion technologies for production of biofuels. Appl Microbiol Biot 96:631–645. https://doi.org/10.1007/s00253-012-4398-0
Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: A review. Renew Sust Energ Rev 14:217–232. https://doi.org/10.1016/j.rser.2009.07.020
Mukhopadhyay N, Ray AK (1999) Utilisation of copra meal in the formulation of compound diets for rohu, Labeo rohita, fingerlings. J Appl Ichthyol 15:127–131. https://doi.org/10.1046/j.1439-0426.1999.00132.x
Nagappan S, Das P, AbdulQuadir M, Thaher M, Khan S, Mahata C, Al-Jabri H, Vatland AK, Kumar G (2021) Potential of microalgae as a sustainable feed ingredient for aquaculture. J Biotechnol 341:1–20. https://doi.org/10.1016/j.jbiotec.2021.09.003
Nandeesha MC, Gangadhar B, Varghese TJ, Keshavanath P (1998) Effect of feeding Spirulina platensis on the growth, proximate composition and organoleptic quality of common carp, Cyprinus carpio L. Aquac Res 29:305–312. https://doi.org/10.1046/j.1365-2109.1998.00163.x
Nandeesha MC, Gangadhara B, Manissery JK, Venkataraman LV (2001) Growth performance of two Indian major carps, catla (Catla catla) and rohu (Labeo rohita) fed diets containing different levels of Spirulina platensis. Bioresource Technol 80:117–120. https://doi.org/10.1016/S0960-8524(01)00085-2
National Research Council (2011) Nutrient requirements of fish and shrimp. National Academies Press, Washington DC
Oh Y-K, Kim S, Ilhamsyah DPA, Lee S-G, Kim JR (2022) Cell disruption and lipid extraction from Chlorella species for biorefinery applications: Recent advances. Bioresource Technol 366:128183. https://doi.org/10.1016/j.biortech.2022.128183
Oliva-Teles A, Enes P, Peres H (2015) Replacing fishmeal and fish oil in industrial aquafeeds for carnivorous fish. In: Davis DA (ed) Feed and feeding practices in aquaculture. Woodhead Publishing, Oxford, pp 203–233
Olvera-Novoa M, Dominguez-Cen L, Olivera-Castillo L, Martínez-Palacios CA (1998) Effect of the use of the microalga Spirulina maxima as fish meal replacement in diets for tilapia, Oreochromis mossambicus (Peters), fry. Aquac Res 29:709–715. https://doi.org/10.1046/j.1365-2109.1998.29100709.x
Pacheco-Vega JM, Gamboa-Delgado J, Alvarado-Ibarra AG, Nieto-López MG, Tapia-Salazar M, Cruz-Suárez LE (2018) Nutritional contribution of fish meal and microalgal biomass produced from two endemic microalgae to the growth of shrimp Penaeus vannamei. Lat Am J Aquat Res 46:53–62. https://doi.org/10.3856/vol46-issue1-fulltext-7
Pakravan S, Akbarzadeh A, Sajjadi MM, Hajimoradloo A, Noori F (2017) Partial and total replacement of fish meal by marine microalga Spirulina platensis in the diet of Pacific white shrimp Litopenaeus vannamei: Growth, digestive enzyme activities, fatty acid composition and responses to ammonia and hypoxia stress. Aquac Res 48:5576–5586. https://doi.org/10.1111/are.13379
Pakravan S, Akbarzadeh A, Sajjadi MM, Hajimoradloo A, Noori F (2018) Chlorella vulgaris meal improved growth performance, digestive enzyme activities, fatty acid composition and tolerance of hypoxia and ammonia stress in juvenile Pacific white shrimp Litopenaeus vannamei. Aquacult Nutr 24:594–604. https://doi.org/10.1111/anu.12594
Palmegiano GB, Agradi E, Forneris G, Gai F, Gasco L, Rigamonti E, Sicuro B, Zoccarato I (2005) Spirulina as a nutrient source in diets for growing sturgeon (Acipenser baeri). Aquac Res 36:188–195. https://doi.org/10.1111/j.1365-2109.2005.01209.x
Palmegiano GB, Gai F, Daprà F, Gasco L, Pazzaglia M, Peiretti PG (2008) Effects of Spirulina and plant oil on the growth and lipid traits of white sturgeon (Acipenser transmontanus) fingerlings. Aquac Res 39:587–595. https://doi.org/10.1111/j.1365-2109.2008.01914.x
Patterson D, Gatlin DM (2013) Evaluation of whole and lipid-extracted algae meals in the diets of juvenile red drum (Sciaenops ocellatus). Aquaculture 416:92–98. https://doi.org/10.1016/j.aquaculture.2013.08.033
Perez-Garcia O, Escalante FME, de-Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: Metabolism and potential products. Water Res 45:11–36. https://doi.org/10.1016/j.watres.2010.08.037
Perez-Velazquez M, Gatlin DM, González-Félix ML, García-Ortega A (2018) Partial replacement of fishmeal and fish oil by algal meals in diets of red drum Sciaenops ocellatus. Aquaculture 487:41–50. https://doi.org/10.1016/j.aquaculture.2018.01.001
Perez-Velazquez M, Gatlin DM, González-Félix ML, García-Ortega A, de Cruz CR, Juárez-Gómez ML, Chen K (2019) Effect of fishmeal and fish oil replacement by algal meals on biological performance and fatty acid profile of hybrid striped bass (Morone crhysops ♀ × M. saxatilis ♂). Aquaculture 507:83–90. https://doi.org/10.1016/j.aquaculture.2019.04.011
Péron G, François Mittaine J, Le Gallic B (2010) Where do fishmeal and fish oil products come from? An analysis of the conversion ratios in the global fishmeal industry. Mar Policy 34:815–820. https://doi.org/10.1016/j.marpol.2010.01.027
Polakof S, Panserat S, Soengas JL, Moon TW (2012) Glucose metabolism in fish: a review. J Comp Physiol 182:1015–1045. https://doi.org/10.1007/s00360-012-0658-7
Posten C (2009) Design principles of photo-bioreactors for cultivation of microalgae. Eng Life Sci 9:165–177. https://doi.org/10.1002/elsc.200900003
Prabakaran G, Moovendhan M, Arumugam A, Matharasi A, Dineshkumar R, Sampathkumar P (2018) Quantitative analysis of phytochemical profile in marine microalgae Chlorella vulgaris. Int J Pharm Biol Sci 8:562–565
Pulz O (2001) Photobioreactors: production systems for phototrophic microorganisms. Appl Microbiol Biot 57:287–293. https://doi.org/10.1007/s002530100702
Qiao H, Hu D, Ma J, Wang X, Wu H, Wang J (2019) Feeding effects of the microalga Nannochloropsis sp. on juvenile turbot (Scophthalmus maximus L.). Algal Res 41:101540. https://doi.org/10.1016/j.algal.2019.101540
Radhakrishnan S, Saravana Bhavan P, Seenivasan C, Muralisankar T (2015) Effect of dietary replacement of fishmeal with Chlorella vulgaris on growth performance, energy utilization and digestive enzymes in Macrobrachium rosenbergii postlarvae. Int J Fish Aquac 7:62–70. https://doi.org/10.5897/IJFA15.0471
Radhakrishnan S, Belal IEH, Seenivasan C, Muralisankar T, Bhavan PS (2016) Impact of fishmeal replacement with Arthrospira platensis on growth performance, body composition and digestive enzyme activities of the freshwater prawn, Macrobrachium rosenbergii. Aquacult Rep 3:35–44. https://doi.org/10.1016/j.aqrep.2015.11.005
Ragaza JA, Hossain MS, Meiler KA, Velasquez SF, Kumar V (2020) A review on Spirulina: alternative media for cultivation and nutritive value as an aquafeed. Rev Aquacult 12:2371–2395. https://doi.org/10.1111/raq.12439
Rahimnejad S, Lee S-M, Park H-G, Choi J (2017) Effects of dietary inclusion of Chlorella vulgaris on growth, blood biochemical parameters, and antioxidant enzyme activity in olive flounder, Paralichthys olivaceus. J World Aquacult Soc 48:103–112. https://doi.org/10.1111/jwas.12320
Raji AA, Junaid OQ, Milow P, Taufek NM, Fada AM, Kolawole AA, Alias Z, Razak SA (2019) Partial replacement of fishmeal with Spirulina platensis and Chlorella vulgaris and its effect on growth and body composition of African catfish Clarias gariepinus (Burchell 1822). Indian J Fish 66:100–111. https://doi.org/10.21077/ijf.2019.66.4.87193-13
Raji AA, Jimoh WA, Abu Bakar NH, Taufek NHM, Muin H, Alias Z, Milow P, Razak SA (2020) Dietary use of Spirulina (Arthrospira) and Chlorella instead of fish meal on growth and digestibility of nutrients, amino acids and fatty acids by African catfish. J Appl Phycol 32:1763–1770. https://doi.org/10.1007/s10811-020-02070-y
Richmond A, Hu Q (2013) Handbook of microalgal culture: applied phycology and biotechnology. John Wiley & Sons, UK
Rincón DD, Velásquez HA, Dávila MJ, Semprun AM, Morales ED, Hernández JL (2012) Substitution levels of fish meal by Arthrospira (=Spirulina) maxima meal in experimental diets for red tilapia fingerlings (Oreochromis sp.). Rev Colomb Cienc Pec 25:430–437
Rizwan M, Mujtaba G, Memon SA, Lee K, Rashid N (2018) Exploring the potential of microalgae for new biotechnology applications and beyond: A review. Renew Sust Energ Rev 92:394–404. https://doi.org/10.1016/j.rser.2018.04.034
Rosas VT, Bessonart M, Romano LA, Tesser MB (2019) Fishmeal substitution for Arthrospira platensis in juvenile mullet (Mugil liza) and its effects on growth and non-specific immune parameters. Rev Colomb Cienc Pec 32:3–13. https://doi.org/10.17533/udea.rccp.v32n1a01
Roy SS, Pal R (2015) Microalgae in aquaculture: a review with special references to nutritional value and fish dietetics. Proc Zool Soc 68:1–8. https://doi.org/10.1007/s12595-013-0089-9
Safi C, Zebib B, Merah O, Pontalier P-Y, Vaca-Garcia C (2014a) Morphology, composition, production, processing and applications of Chlorella vulgaris: A review. Renew Sust Energ Rev 35:265–278. https://doi.org/10.1016/j.rser.2014.04.007
Safi C, Ursu AV, Laroche C, Zebib B, Merah O, Pontalier P-Y, Vaca-Garcia C (2014b) Aqueous extraction of proteins from microalgae: Effect of different cell disruption methods. Algal Res 3:61–65. https://doi.org/10.1016/j.algal.2013.12.004
Samtiya M, Aluko RE, Dhewa T (2020) Plant food anti-nutritional factors and their reduction strategies: an overview. Food Prod Process Nutr 2:6. https://doi.org/10.1186/s43014-020-0020-5
Sarker PK, Kapuscinski AR, Bae AY, Donaldson E, Sitek AJ, Fitzgerald DS, Edelson OF (2018) Towards sustainable aquafeeds: Evaluating substitution of fishmeal with lipid-extracted microalgal co-product (Nannochloropsis oculata) in diets of juvenile Nile tilapia (Oreochromis niloticus). PLoS One 13:e0201315. https://doi.org/10.1371/journal.pone.0201315
Sarker PK, Kapuscinski AR, McKuin B, Fitzgerald DS, Nash HM, Greenwood C (2020) Microalgae-blend tilapia feed eliminates fishmeal and fish oil, improves growth, and is cost viable. Sci Rep 10:19328. https://doi.org/10.1038/s41598-020-75289-x
Sauvant D, Perez J-M, Tran G, Ponter AA (2004) Tables of composition and nutritional value of feed materials: pigs, poultry, cattle, sheep, goats, rabbits, horses and fish. Wageningen Academic, France
Scholz MJ, Weiss TL, Jinkerson RE, Jing J, Roth R, Goodenough U, Posewitz MC, Gerken HG (2014) Ultrastructure and composition of the Nannochloropsis gaditana cell wall. Eukaryot Cell 13:1450–1464. https://doi.org/10.1128/EC.00183-14
Sheih IC, Fang TJ, Wu T-K (2009) Isolation and characterisation of a novel angiotensin I-converting enzyme (ACE) inhibitory peptide from the algae protein waste. Food Chem 115:279–284. https://doi.org/10.1016/j.foodchem.2008.12.019
Shepherd C, Jackson A (2013) Global fishmeal and fish-oil supply: inputs, outputs and marketsa. J Fish Biol 83:1046–1066. https://doi.org/10.1111/jfb.12224
Shi X, Luo Z, Chen F, Wei C-C, Wu K, Zhu X-M, Liu X (2017) Effect of fish meal replacement by Chlorella meal with dietary cellulase addition on growth performance, digestive enzymatic activities, histology and myogenic genes’ expression for crucian carp Carassius auratus. Aquac Res 48:3244–3256. https://doi.org/10.1111/are.13154
Shiau SY, Chuang JL, Sun CL (1987) Inclusion of soybean meal in tilapia (Oreochromis aureus×O.niloticus) diets at two protein levels. Aquaculture 65:251–261. https://doi.org/10.1016/0044-8486(87)90238-9
Shubert E, Gärtner G (2015) Nonmotile coccoid and colonial green algae. In: Wehr JD, Sheath RG, Kociolek JP (eds) Freshwater algae of North America, 3rd edn. Academic Press, Boston, pp 315–373
Silva AJ, Cavalcanti VLR, Porto ALF, Gama WA, Brandão-Costa RMP, Bezerra RP (2020) The green microalgae Tetradesmus obliquus (Scenedesmus acutus) as lectin source in the recognition of ABO blood type: purification and characterization. J Appl Phycol 32:103–110. https://doi.org/10.1007/s10811-019-01923-5
Sims S, Ajayi O, Roubach R (2019) Microalgae in aquatic animal feeds. FAO Aquacult Newslett 60:50–50
Sinha AK, Kumar V, Makkar HPS, De Boeck G, Becker K (2011) Non-starch polysaccharides and their role in fish nutrition – A review. Food Chem 127:1409–1426. https://doi.org/10.1016/j.foodchem.2011.02.042
Sivakumar N, Sundararaman M, Selvakumar G (2018) Evaluation of growth performance of Penaeus monodon (Fabricius) fed diet with partial replacement of fishmeal by Spirulina platensis (Sp) meal. Indian J Anim Res 52:1721–1726. https://doi.org/10.18805/ijar.B-3438
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. https://doi.org/10.1016/j.aquaculture.2016.04.010
Sørensen M, Gong Y, Bjarnason F, Vasanth GK, Dahle D, Huntley M, Kiron V (2017) Nannochloropsis oceania-derived defatted meal as an alternative to fishmeal in Atlantic salmon feeds. PLoS One 12:e0179907. https://doi.org/10.1371/journal.pone.0179907
Stone DAJ (2003) Dietary carbohydrate utilization by fish. Rev Fish Sci 11:337–369. https://doi.org/10.1080/10641260390260884
Suarez Ruiz CA, Baca SZ, van den Broek LAM, van den Berg C, Wijffels RH, Eppink MHM (2020) Selective fractionation of free glucose and starch from microalgae using aqueous two-phase systems. Algal Res 46:101801. https://doi.org/10.1016/j.algal.2020.101801
Subasinghe R, Soto D, Jia J (2009) Global aquaculture and its role in sustainable development. Rev Aquacult 1:2–9. https://doi.org/10.1111/j.1753-5131.2008.01002.x
Sucunthowong K, Lee JH, Powtongsook S, Nootong K (2023) Simultaneous utilization of CO2 and nitrate wastes from compact recirculating aquaculture system for improving algal biomass (Scenedesmus armatus) production. Algal Res 74:103224. https://doi.org/10.1016/j.algal.2023.103224
Sultana R, Khatoon H, Rahman MR, Haque ME, Nayma Z, Mukta FA (2022) Potentiality of Nannochloropsis sp. as partial dietary replacement of fishmeal on growth, proximate composition, pigment and breeding performance in guppy (Poecilia reticulata). Bioresour Technol Rep 18:101112. https://doi.org/10.1016/j.biteb.2022.101112
Tacon AGJ (2020) Trends in global aquaculture and aquafeed production: 2000–2017. Rev Fish Sci Aquac 28:43–56. https://doi.org/10.1080/23308249.2019.1649634
Tacon AG, Metian MR, Tacon MAG, Hasan MR, Metian M (2011) Demand and supply of feed ingredients for farmed fish and crustaceans: trends and prospects. Food and Agriculture Organization of the United Nations (FAO), Rome
Teimouri M, Amirkolaie AK, Yeganeh S (2013) The effects of Spirulina platensis meal as a feed supplement on growth performance and pigmentation of rainbow trout (Oncorhynchus mykiss). Aquaculture 396–399:14–19. https://doi.org/10.1016/j.aquaculture.2013.02.009
Teuling E, Schrama JW, Gruppen H, Wierenga PA (2017) Effect of cell wall characteristics on algae nutrient digestibility in Nile tilapia (Oreochromis niloticus) and African catfish (Clarus gariepinus). Aquaculture 479:490–500. https://doi.org/10.1016/j.aquaculture.2017.06.025
Teves JFC, Ragaza JA (2016) The quest for indigenous aquafeed ingredients: a review. Rev Aquacult 6:1–18. https://doi.org/10.1111/raq.12089
Tham PE, Lim HR, Khoo KS, Chew KW, Yap YJ, Munawaroh HSH, Ma Z, Rajendran S, Gnanasekaran L, Show PL (2023) Insights of microalgae-based aquaculture feed: A review on circular bioeconomy and perspectives. Algal Res 74:103186. https://doi.org/10.1016/j.algal.2023.103186
Tomas-Almenar C, Larran AM, de Mercado E, Sanz-Calvo MA, Hernandez D, Riano B, Garcia-Gonzalez MC (2018) Scenedesmus almeriensis from an integrated system waste-nutrient, as sustainable protein source for feed to rainbow trout (Oncorhynchus mykiss). Aquaculture 497:422–430. https://doi.org/10.1016/j.aquaculture.2018.08.011
Tongsiri S, Mang-Amphan K, Peerapornpisal Y (2010) Effect of replacing fishmeal with Spirulina on growth, carcass composition and pigment of the Mekong giant catfish. Asian J Agric Sci 2:106–110
Torstensen BE, Espe M, Sanden M, Stubhaug I, Waagbø R, Hemre GI, Fontanillas R, Nordgarden U, Hevrøy EM, Olsvik P, Berntssen MHG (2008) Novel production of Atlantic salmon (Salmo salar) protein based on combined replacement of fish meal and fish oil with plant meal and vegetable oil blends. Aquaculture 285:193–200. https://doi.org/10.1016/j.aquaculture.2008.08.025
Trainor FR, Cain JR, Shubert LE (1976) Morphology and nutrition of the colonial green alga Scenedesmus: 80 years later. Bot Rev 42:5–25. https://doi.org/10.1007/BF02860860
Transparency Market Research (2016) Algae market (by application, by cultivation technology, and geography) – Global industry analysis, size, share, growth, trends, and forecast 2016–2024. Transparency Market Research. https://www.transparencymarketresearch.com/algae-market.html. Accessed 5 Dec 2017
Valente LMP, Custódio M, Batista S, Fernandes H, Kiron V (2019) Defatted microalgae (Nannochloropsis sp.) from biorefinery as a potential feed protein source to replace fishmeal in European sea bass diets. Fish Physiol Biochem 45:1067–1081. https://doi.org/10.1007/s10695-019-00621-w
Van Binh V, Siddik MAB, Fotedar R, Chaklader MR, Abu Hanif M, Foysal MJ, Huy Quang N (2020) Progressive replacement of fishmeal by raw and enzyme-treated alga, Spirulina platensis influences growth, intestinal micromorphology and stress response in juvenile barramundi, Lates calcarifer. Aquaculture 529:73541. https://doi.org/10.1016/j.aquaculture.2020.735741
Vassiliou V, Charalambides M, Menicou M, Chartosia N, Tzen E, Evagelos B, Papadopoulos P, Loucaides A (2015) Aquaculture feed management system powered by renewable energy sources: investment justification. Aquacult Econ Manag 19:423–443. https://doi.org/10.1080/13657305.2015.1082115
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. https://doi.org/10.1007/s10811-015-0661-y
Velazquez-Lucio J, Rodríguez-Jasso RM, Colla LM, Sáenz-Galindo A, Cervantes-Cisneros DE, Aguilar CN, Fernandes BD, Ruiz HA (2018) Microalgal biomass pretreatment for bioethanol production: a review. Biofuel Res J 5:780–791. https://doi.org/10.18331/brj2018.5.1.5
Vizcaíno AJ, López G, Sáez MI, Jiménez JA, Barros A, Hidalgo L, Camacho-Rodríguez J, Martínez TF, Cerón-García MC, Alarcón FJ (2014) Effects of the microalga Scenedesmus almeriensis as fishmeal alternative in diets for gilthead sea bream, Sparus aurata, juveniles. Aquaculture 431:34–43. https://doi.org/10.1016/j.aquaculture.2014.05.010
Vonshak A (1997) Spirulina platensis (Arthrospira): physiology, cell-biology and biotechnology. CRC Press, London
Walker AB, Berlinsky DL (2011) Effects of partial replacement of fish meal protein by microalgae on growth, feed Intake, and body composition of Atlantic cod. N Am J Aquacult 73:76–83. https://doi.org/10.1080/15222055.2010.549030
Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329:796–799. https://doi.org/10.1126/science.1189003
Wu L-c, J-aA Ho, Shieh M-C, Lu I-W (2005) Antioxidant and antiproliferative activities of Spirulina and Chlorella water extracts. J Agr Food Chem 53:4207–4212. https://doi.org/10.1021/jf0479517
Xi L, Lu Q, Liu Y, Su J, Chen W, Gong Y, Han D, Yang Y, Zhang Z, Jin J, Liu H, Zhu X, Xie S (2022) Effects of fish meal replacement with Chlorella meal on growth performance, pigmentation, and liver health of largemouth bass (Micropterus salmoides). Anim Nutr 10:26–40. https://doi.org/10.1016/j.aninu.2022.03.003
Xiao X, Zhou Y, Liang Z, Lin R, Zheng M, Chen B, He Y (2022) A novel two-stage heterotrophic cultivation for starch-to-protein switch to efficiently enhance protein content of Chlorella sp. MBFJNU-17. Bioresour Technol 344:126187. https://doi.org/10.1016/j.biortech.2021.126187
Xie T, Xia Y, Zeng Y, Li X, Zhang Y (2017) Nitrate concentration-shift cultivation to enhance protein content of heterotrophic microalga Chlorella vulgaris: Over-compensation strategy. Bioresour Technol 233:247–255. https://doi.org/10.1016/j.biortech.2017.02.099
Yamada T, Sakaguchi K (1982) Comparative studies onChlorella cell walls: Induction of protoplast formation. Arch Microbiol 132:10–13. https://doi.org/10.1007/BF00690809
Yamamoto T, Shima T, Furuita H, Suzuki N, Shiraishi M (2001) Nutrient digestibility values of a test diet determined by manual feeding and self-feeding in rainbow trout and common carp. Fish Sci 67:355–357. https://doi.org/10.1046/j.1444-2906.2001.00251.x
Yang L, Li H, Lu Q, Zhou W (2021) Emerging trends of culturing microalgae for fish-rearing environment protection. J Chem Technol Biot 96:31–37. https://doi.org/10.1002/jctb.6563
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Great thanks were given to Qiang Hu for his instructive suggestions for the review.
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This work was supported by the Doctoral Scientific Research Foundation of Henan University of Science and Technology (13480087; 13480088), Henan Provincial Science and Technology Research Project (222102320144), and the National Natural Science Foundation of China (NSFC, no. 32202952).
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Gao, S., Chen, W., Cao, S. et al. Microalgae as fishmeal alternatives in aquaculture: current status, existing problems, and possible solutions. Environ Sci Pollut Res 31, 16113–16130 (2024). https://doi.org/10.1007/s11356-024-32143-1
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DOI: https://doi.org/10.1007/s11356-024-32143-1