Develando el potencial de las algas para la elaboración de piensos para peces de acuicultura
Palabras clave:
algas, compuestos bioactivos, ingredientes alternativos, peces marinos, piensosResumen
El desarrollo de piensos acuícolas sostenibles sigue siendo uno de los mayores desafíos de la acuicultura. En las últimas décadas se ha realizado un gran esfuerzo de investigación en la evaluación de ingredientes alternativos para poder reducir la dependencia sobre los ingredientes convencionales. Estos ingredientes alternativos deben de tener un valor nutricional adecuado, tener una buena disponibilidad para permitir su uso a escala industrial y ser económicamente asequibles. En este sentido, el uso de algas en piensos para acuicultura despierta un gran interés, principalmente por su composición nutricional y enorme variedad de compuestos bioactivos que contienen, así como por los beneficios que generan en los peces, como son la mejora del crecimiento, la composición proximal del músculo y funcionalidad digestiva, tal y como se evidencia en las numerosas publicaciones científicas al respecto. Sin embargo, existen ciertos aspectos que deben de considerarse para que la industria de elaboración de pienso de acuicultura pueda incorporarlas como ingredientes o aditivos en las fórmulas comerciales a gran escala, como son todos aquellos relacionados con la seguridad y las normativas regulatorias, la reducción de sus costes de producción, la variabilidad en su composición química, una mayor bioaccesibilidad de los nutrientes que contienen, o la presencia de factores antinutritivos, entre otros. Por lo tanto, en este trabajo se recopila información sobre la composición nutricional de las algas, y datos de estudios publicados en los que se describen sus efectos en los peces cuando se usan como ingrediente o como aditivo funcional en los piensos. Además, se discuten los principales retos para su uso generalizado en piensos comerciales y las perspectivas futuras.
Descargas
Citas
Adams C, Godfrey V, Wahlen B, Seefeldt L & Bugbee B (2013) Understanding precision nitrogen stress to optimize the growth and lipid content trade off in oleaginous green microalgae. Bioresource Technology 131, 188–194. DOI: 10.1016/j.biortech.2012.12.143
Alarcón FJ, Díaz M, Moyano FJ & Abellán E (1998) Characterization and functional properties of digestive proteases in two sparids; gilthead sea bream (Sparus aurata) and common dentex (Dentex dentex). Fish Physiology and Biochemistry 19, 257–267. DOI: 10.1023/A:1007717708491
Arasaki S & Arasaki T (1983) Low calorie, high nutrition vegetables from the sea. To help you look and feel better. Japan Publications, Tokyo. Inc pp. (1), 6–196.
Becker EW (1994) Microalgae: Biotechnology and Microbiology. Cambridge: Cambridge University Press.
Becker E (2007) Micro-algae as a source of protein. Biotechnology Advances 25, 207–210.
Bernaerts TMM, Gheysen L, Kyomugasho C, Jamsazzadeh Kermani Z, Vandionant S, Foubert I, Hendrickx ME & Van Loey AM (2018) Comparison of microalgal biomasses as functional food ingredients: Focus on the composition of cell wall related polysaccharides. Algal Research 32, 150–161. DOI: 10.1016/j.algal.2018.03.017
Booman M, Forster I, Vederas JC, Groman DB & Jones SRM (2018) Soybean meal-induced enteritis in Atlantic salmon (Salmo salar) and Chinook salmon (Oncorhynchus tshawytscha) but not in pink salmon (O. gorbuscha). Aquaculture 483, 238–243. DOI: 10.1016/j.aquaculture.2017.10.025
Brown MR (2002) Nutritional value and use of microalgae in aquaculture. Avances en Nutrición Acuícola VI. Memorias del VI Simposium Internacional de Nutrición Acuícola 3, 281–292.
Brown MR, Jeffrey SW, Volkman JK & Dunstan GA (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151, 315-331. DOI: 10.1016/S0044-8486(96)01501-3
Canales-Gómez E, Correa G & Viana MT (2010) Effect of commercial carotene pigments (astaxanthin, cantaxanthin and β-carotene) in juvenile abalone Haliotis rufescens diets on the color of the shell of nacre. Veterinaria Mexico 41, 191–200.
Cardoso C, Ripol A, Afonso C, Freire M, Varela J, Quental‐Ferreira H, Pousão-Ferreira P & Bandarra N (2017) Fatty acid profiles of the main lipid classes of green seaweeds from fishpond aquaculture. Food Science and Nutrition 5(6), 1186–1194. DOI: 10.1002/fsn3.511
Carvalho M, Montero D, Rosenlund G, Fontanillas R, Ginés R & Izquierdo M (2020) Effective complete replacement of fish oil by combining poultry and microalgae oils in practical diets for gilthead sea bream (Sparus aurata) fingerlings. Aquaculture 529, 735696. DOI: 10.1016/j.aquaculture.2020.735696
Cerezuela R, Fumanal M, Tapia-Paniagua ST, Meseguer J, Moriñigo MA & Esteban MA (2012) Histological alterations and microbial ecology of the intestine in gilthead seabream (Sparus aurata L.) fed dietary probiotics and microalgae. Cell Tissue Research 350, 477–489. DOI: 10.1007/s00441-012-1495-4
Chisti Y (2007) Biodiesel from microalgae. Biotechnology Advances 25(3), 294–306. DOI: 10.1016/j.biotechadv.2007.02.001
Cian RE, Martínez-Augustin O & Drago SR (2012) Bioactive properties of peptides obtained by enzymatic hydrolysis from protein byproducts of Porphyra columbina. Food Research International 49, 364–372. DOI: 10.1016/j.foodres.2012.07.003
Cruz-Suárez LE, Tapia-Salazar M, Nieto-López MG, Guajardo-Barbosa C & Ricque-Marie D (2009) Comparison of Ulva clathrata and the kelps Macrocystis pyrifera and Ascophyllum nodosum as ingredients in shrimp feeds. Aquaculture Nutrition 15, 421–430. DOI: 10.1111/j.1365-2095.2008.00607.x
Cuellar-Bermudez SP, Aguilar-Hernandez I, Cardenas-Chavez DL, Ornelas-Soto N, Romero-Ogawa MA & Parra-Saldivar R (2015) Extraction and purification of high-value metabolites from microalgae: Essential lipids, astaxanthin and phycobiliproteins. Microbiology Biotechnology 8, 190–209. DOI: 10.1111/1751-7915.12167
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. Bioresource Technology 98, 1433–1439. DOI: 10.1016/j.biortech.2006.05.043
Daniel N (2018) A review on replacing fishmeal in aqua feeds using plant protein sources. International Journal of Fisheries and Aquatic Studies 6(2), 164–179.
Del Campo JA, Rodríguez H, Moreno J, Vargas MA, Rivas J & Guerrero MG (2004) Accumulation of astaxanthin and lutein in Chlorella zofingiensis (Chlorophyta). Applied Microbiology and Biotechnololgy 64, 848–854. DOI: 10.1007/s00253-003-1510-5
Di Lena G, Casini I, Lucarini M, del Pulgar JS, Aguzzi A, Caproni R, Gabrielli P & Lombardi-Boccia G (2020) Chemical characterization and nutritional evaluation of microalgal biomass from large-scale production: a comparative study of five species. European Food Research and Technology 246(2), 323–332. DOI: 10.1007/s00217-019-03346-5
Diken G, Demir O & Naz M (2016) The inhibitory effects of different diets on the protease activities of Argyrosomus regius (Pisces, Scianidae) larvae as a potential candidate species. Journal of Applied Animal Research 46(1), 1–6. DOI: 10.1080/09712119.2016.1263200
Dunstan GA, Volkman JK, Jeffrey SW & Barrett SM (1992) Biochemical composition of microalgae from the green algal classes Chlorophyceae and Prasinophyceae. 2. Lipid classes and fatty acids. Journal of Experimental Marine Biology and Ecology 161(1), 115–134. DOI: 10.1016/0022-0981(92)90193-E
Enzing C, Ploeg M & Barbosa M (2014) Microalgae-based products for the food and feed sector: an outlook for Europe. IPTS Inst.
European Food Safety Authority (EFSA) (2011) Guidance on the assessment of microbial biomasses for use in animal nutrition. EFSA Journal 9(3), 2117
Ergün S, Soyutürk M, Güroy B, Güroy D & Merrifield, D (2009) Influence of Ulva meal on growth, feed utilization, and body composition of juvenile Nile tilapia (Oreochromis niloticus) at two levels of dietary lipid. Aquaculture International 17(4), 355. DOI: 10.1007/s10499-008-9207-5
FAO (2020) The State of World Fisheries and Aquaculture 2020. Sustainability in action. Rome. https://doi.org/10.4060/ca9229en
Galafat A, Vizcaíno AJ, Sáez MI, Martínez TF, Jerez-Cepa I, Mancera JM & Alarcón FJ (2020) Evaluation of Arthrospira sp. enzyme hydrolysate as dietary additive in gilthead seabream (Sparus aurata) juveniles. Journal of Applied Phycology 32, 3089–3100. DOI: 10.1007/s10811-020-02141-0
Galland-Irmouli AV, Fleurence J, Lamghari R, Luçon M, Rouxel C, Barbaroux O, Bronowicki JP, Villaume C & Gueant JL (1999) Nutritional value of proteins from edible seaweed Palmaria palmata (dulse). The Journal of Nutritional Biochemistry 10, 353–359. DOI: 10.1016/s0955-2863(99)00014-5
García‐Márquez J, Rico RM, Sánchez‐Saavedra MDP, Gómez-Pinchetti JL, Acién FG, Figueroa FL, Alarcón FJ, Moriñigo MA & Abdala-Díaz RT (2020) A short pulse of dietary algae boosts immune response and modulates fatty acid composition in juvenile Oreochromis niloticus. Aquaculture Research 51, 4397–4409. DOI: 10.1111/are.14781
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. DOI: 10.1016/J.AQUACULTURE.2018.11.049
Gora AH, Ambasankar K, Sandeep KP, Rehman S, Agarwal D, Ahmad L & Ramachandran K (2019) Effect of dietary supplementation of crude microalgal extracts on growth performance, survival and disease resistance of Lates calcarifer (Bloch, 1790) larvae. Indian Journal of Fisheries 66, 64–72. DOI: 10.21077/ijf.2019.66.1.79076-09
Gressler V, Yokoya NS, Fujii MT, Colepicolo P, Mancini Filho J, Torres RP & Pinto E (2010) Lipid, fatty acid, protein, amino acid and ash contents in four Brazilian red algae species. Food Chemistry 120(2), 585–590. DOI: 10.1016/j.foodchem.2009.10.028
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). Journal of Applied Phycology 28, 1011. DOI: 10.1007/s10811-015-0622-5
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). Journal of Fisheries International 7, 61–64. DOI: 10.3923/jfish.2012.61.64
Ivanova V, Stancheva M & Petrova D (2013) Fatty acid composition of black sea Ulva rigida and Cystoseira crinita. Bulgarian Journal of Agricultural Science 19(S1), 42–47.
Joubert Y & Fleurence J (2008) Simultaneous extraction of proteins and DNA by an enzymatic treatment of the cell wall of Palmaria palmata (Rhodophyta). Journal of Applied Phycology 20, 55–61. DOI: 10.1007/s10811-007-9180-9
Kent M, Welladsen HM, Mangott A & Li Y (2015) Nutritional evaluation of Australian microalgae as potential human health supplements. PloS One 10, 2. DOI: 10.1371/journal.pone.0118985
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. Frontiers in Marine Science 3, 67. DOI: 10.3389/fmars.2016.00067
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. Journal of Nutritional Science,4, e24. DOI: 10.1017/jns.2015.14
Kovač DJ, Simeunović JB, Babić OB, Mišan AC & Milovanović IL (2013) Algae in food and feed. Food and Feed Research 40(1), 21–31. DOI: 10.2791/3339
Lers A, Biener Y & Zamir A (1990) Photoinduction of massive beta-carotene accumulation by the alga Dunaliella bardawil: kinetics and dependence on gene activation. Plant Physiology 93, 389–95. DOI: 10.1104/pp.93.2.389
Liu C, Liu H, Han D, Xie S, Jin J, Yang Y & Zhu X. (2020) Effects of dietary Arthrospira platensis supplementation on the growth performance, antioxidation and immune related-gene expression in yellow catfish (Pelteobagrus fulvidraco). Aquaculture Reports 17, 100297. DOI: 10.1016/j.aqrep.2020.100297
López CV, Cerón MC, Acién FG, Segovia C, Chisti Y & Fernández JM (2010) Protein measurements of microalgal and cyanobacterial biomass. Bioresource Technology 101, 7587–7591. DOI: 10.1016/j.biortech.2010.04.077
Mæhre HK (2015) Seaweed proteins–how to get to them? Effects of processing on nutritional value, bioaccessibility and extractability. Tesis Doctoral. Norwegian College of Fishery Science, Faculty of Biosciences, Fisheries and Economics. The Arctic University of Norway.
Mai K, Wan J, Ai Q, Xu W, Liufu Z, Zhang L, Zhang C & Li H (2006a) Dietary methionine requirement of large yellow croaker, Pseudosciaena crocea R. Aquaculture 253(1-4), 564–572. DOI: 10.1016/j.aquaculture.2005.08.010
Mai K, Zhang L, Ai Q, Duan Q, Zhang C, Li H, Wan J & Liufu Z (2006b) Dietary lysine requirement of juvenile Japanese seabass, Lateolabrax japonicus. Aquaculture 258(1-4), 535–542. DOI: 10.1016/j.aquaculture.2006.04.043
Marrion O, Schwertz A, Fleurence J, Gueant JL & Villaume C (2003) Improvement of the digestibility of the proteins of the red alga Palmaria palmata by physical processes and fermentation. Molecular Nutrition Food Research 47, 339–344. DOI: 10.1002/food.200390078
Marsham S, Scott GW & Tobin ML (2007) Comparison of nutritive chemistry of a range of temperate seaweeds. Food Chemistry 100, 1331–1336. DOI: 10.1016/j.foodchem.2005.11.029
McDermid KJ & Stuercke B. (2003) Nutritional composition of edible Hawaiian seaweeds. Journal of Applied Phycology 15, 513–524. DOI: 10.1023/B:JAPH.0000004345.31686.7f
Molino A, Iovine A, Casella P, Mehariya S, Chianese S, Cerbone A, Rimauro J & Musmarra D (2018) Microalgae characterization for consolidated and new application in human food, animal feed and nutraceuticals. International Journal of Environmental Research and Public Health 15(11), 2436. DOI: 10.3390/ijerph15112436
Mourente G, Lubian LM & Odriozola JM (1990) Total fatty acid composition as a taxonomic index of some marine microalgae used as food in marine aquaculture. Hydrobiologia 203(3), 147–154. DOI: 10.1007/BF00005683
Moutinho S, Linares F, Rodriguez JL, Vera Sousa & Valente LMP (2018) Inclusion of 10% seaweed meal in diets for juvenile and on-growing life stages of Senegalese sole (Solea senegalensis). Journal of Applied Phycology 30(6), 3589–3601. DOI: 10.1007/s10811-018-1482-6
Nakagawa K, Kiko T, Miyazawa T, Burdeos GC, Kimura F, Satoh A & Miyazawa T (2011) Antioxidant effect of astaxanthin on phospholipid peroxidation in human erythrocytes. British Journal of Nutrition 105(11), 1563–1571. DOI: 10.1017/S0007114510005398
Naylor RL, Hardy RW, Bureau DP, Chiu A, Elliott M, Farrell AP, Forster I, Gatlin DM, Goldburg RJ, Hua K & Nichols PD (2009) Feeding aquaculture in an era of finite resources. Proceedings of the National Academy of Sciences 106(36), 15103–15110. DOI: 10.1073/pnas.0905235106
Norsker NH, Barbosa MJ, Vermuë MH & Wijffels RH (2011) Microalgal production – a close look at the economics. Biotechnology Advances 29, 24–27. DOI: 10.1016/j.biotechadv.2010.08.005
Oliveira MN, Ponte-Freitas AL, Urano-Carvalho AF, Taveres-Sampaio TM, Farias DF, Alves-Teixera DI, Gouveia ST, Gomes-Pereira J & Castro-Catanho de Sena MM (2009) Nutritive and non-nutritive attributes of washed-up seaweeds from the coast of Ceará, Brazil. Food Chemistry 11, 254–259. DOI: 10.1016/j.foodchem.2008.12.004
Ortiz J, Romero N & Robert P (2006) Dietary fiber, amino acid, fatty acid and tocopherol contents of the edible seaweeds Ulva lactuca and Durvillaea antarctica. Food Chemistry 99(1), 98–104. DOI: 10.1016/j.foodchem.2005.07.027
Percival EE & Turvey JR (1974) Polysaccharides of algae. CRC, handbook of microbiology, condensed edition, 532nd ed, ed. AL Laskin, and HA Lechevalier. Cleveland: CRC Press Inc.
Perera E, Sánchez-Ruiz D, Sáez MI, Galafat A, Barany A, Fernández-Castro M, Vizcaíno AJ, Fuentes J, Martínez TF, Mancera JM, Alarcón FJ & Martos-Sitcha JA (2020) Low dietary inclusion of nutraceuticals from microalgae improves feed efficiency and modifies intermediary metabolisms in gilthead sea bream (Sparus aurata). Scientific Report 10, 18676. DOI: 10.1038/s41598-020-75693-3
Pereira H, Sardinha M, Santos T, Gouveia L, Barreira L, Dias J & Varela J (2020) Incorporation of defatted microalgal biomass (Tetraselmis sp. CTP4) at the expense of soybean meal as a feed ingredient for juvenile gilthead seabream (Sparus aurata). Algal Research 47, 101869. DOI: 10.1016/j.algal.2020.101869
Prabhu KS, Siveen KS, Kuttikrishnan S, Iskandarani A, Tsakou M, Achkar IW, Therachiyil L, Krishnankutty R, Parray A, Kulinski M, Merhi M, Dermime S, Mohammad RM & Uddin S (2017) Targeting of X-linked inhibitor of apoptosis protein and PI3-kinase/AKT signaling by embelin suppresses growth of leukemic cells. PLoS One 12, e0180895. DOI: 10.1371/journal.pone.0180895
Pratoomyot J, Srivilas P & Noiraksar T (2005) Fatty acids composition of 10 microalgal species. Songklanakarin Journal of Science and Technology 27(6), 1179–1187.
Rahimnejad S, Lee SM, Park HG & Choi J (2017) Effects of dietary inclusion of Chlorella vulgaris on growth, blood biochemical parameters, and antioxidant enzyme activity in olive flounder, Paralichthys olivaceus. Journal of the World Aquaculture Society 48(1), 103–112. DOI: 10.1111/jwas.12320
Ren LJ, Ji XJ Huang H., Qu L., Feng Y., Tong Q.Q. & Ouyang P.K. (2010) Development of a stepwise aeration control strategy for efficient docosahexaenoic acid production by Schizochytrium sp. Applied Microbiology and Biotechnology 87(5), 1649–1656. DOI: 10.1007/s00253-010-2639-7
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.). Revista Colombiana de Ciencias Pecuarias 25(3), 430–437.
Roohani AM, Kenari AA, Kapoorchali MF, Borani MS, Zorriehzahra MJ, Smiley AH, Esmaili M & Rombenso AN (2019) Effect of spirulina Spirulina platensis as a complementary ingredient to reduce dietary fishmeal on the growth performance, whole‐body composition, fatty acid and amino acid profiles, and pigmentation of Caspian brown trout (Salmo trutta caspius) juveniles. Aquaculture Nutrition 25, 633–645. DOI: 10.1111/anu.12885
Roy SS & Pal S (2015) Microalgae in aquaculture: a review with special emphasis to nutritional value and fish dietetics. Proceedings of the Zoological Society 68, 1-8. DOI: 10.1007/s12595-013-0089-9
Sáez MI, Martínez TF & Alarcón FJ (2013) Effect of the dietary of seaweeds on intestinal proteolytic activity of juvenile sea bream, Sparus aurata. International Aquafeed 16(2), 38–40.
Sáez MI, Vizcaíno A, Galafat A, Anguís V, Fernández-Díaz C, Balebona MC, Alarcón FJ & Martínez TF (2020) Assessment of long-term effects of the macroalgae Ulva ohnoi included in diets on Senegalese sole (Solea senegalensis) fillet quality. Algal Research 47, 101885. DOI: 10.1016/j.algal.2020.101885
Sahu A, Pancha I, Jain D, Paliwal C, Ghosh T, Patidar S, Bhattacharya S & Mishra S (2013) Fatty acids as biomarkers of microalgae. Phytochemistry 89, 53–58. DOI: 10.1016/j.phytochem.2013.02.001
Sales R, Cerón-García MC, Navarro-López E, González-López C, Tsuzuki MY, Acién-Fernández FG, Alarcón FJ & Molina-Grima E (2020) Processing Nannochloropsis gaditana biomass for the extraction of high-value biocompounds. Journal of Applied Phycology 32, 3113–3122. DOI: 10.1007/s10811-020-02156-7
Sánchez JF, Fernández JM, Acién FG, Rueda A, Pérez-Parra J & Molina E (2008) Influence of culture conditions on the productivity and lutein content of the new strain Scenedesmus almeriensis. Process Biochemistry 43, 398–405.DOI: 10.1016/j.procbio.2008.01.004
Santigosa E, Sáez de Rodrigáñez MA, Rodiles A, García-Barroso F & Alarcón FJ (2010) Effect of diets containing a purified soybean trypsin inhibitor on growth performance, digestive proteases and intestinal histology in juvenile sea bream (Sparus aurata L.). Aquaculture Research 41, e187-e198. DOI: 10.1111/j.1365-2109.2010.02500.x
Sarker PK, Gamble MM, Kelson S & Kapuscinski AR (2016) 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. Aquaculture Nutrition 22(1), 109–119. DOI: 10.1111/anu.12230
Servel MO, Claire C, Derrien A, Coiffard L & De Roeck-Holtzhauer Y (1994) Fatty acid composition of some marine microalgae. Phytochemistry 36(3), 691–693. DOI: 10.1016/S0031-9422(00)89798-8
Shah MMR, Liang Y, Cheng JJ & Daroch M (2016) Astaxanthin-producing green microalga Haematococcus pluvialis: from single cell to high value commercial products. Frontiers in Plant Science 7, 531. DOI: 10.3389/fpls.2016.00531
Shah MR, Lutzu GA, Alam A, Sarker P. Chowdhury MK, Parsaeimehr A, Liang Y & Daroch M (2018) Microalgae in aquafeeds for a sustainable aquaculture industry. Journal of Applied Phycology 30(1), 197–213. DOI: 10.1007/s10811-017-1234-z
Shi X, Luo Z, Chen F, Wei CC, Wu K, Zhu XM & 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. Aquaculture Research 48, 3244–3256. DOI: 10.1111/are.13154
Shields RJ & Lupatsch I (2012) Algae for aquaculture and animal feeds. TATuP-Zeitschrift für Technikfolgenabschätzung in Theorie und Praxis 21, 23–37. DOI: 10.14512/tatup.21.1.23
Shuuluka D, Bolton JJ & Anderson RJ (2013) Protein content, amino acid composition and nitrogen-to-protein conversion factors of Ulva rigida and Ulva capensis from natural populations and Ulva lactuca from an aquaculture system, in South Africa. Journal of Applied Phycology 25(2), 677–685. DOI: 10.1007/s10811-012-9902-5
Silva DM, Valente LMP, Sousa-Pinto I, Pereira R, Pires MA, Seixas F & Rema P (2015) Evaluation of IMTA-produced seaweeds (Gracilaria, Porphyra, and Ulva) as dietary ingredients in Nile tilapia, Oreochromis niloticus L., juveniles. Effects on growth performance and gut histology. Journal of Applied Phycology 27, 1671–1680. DOI: 10.1007/s10811-014-0453-9
Slocombe SP, Ross M, Thomas N, McNeill S & Stanley MS (2013) A rapid and general method for measurement of protein in micro-algal biomass. Bioresource Technology 129, 51–57. DOI: 10.1016/j.biortech.2012.10.163
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. DOI: 10.1016/j.aquaculture.2016.04.010
Spolaore P, Joannis-Cassan C, Duran E & Isambert A (2006) Commercial applications of microalgae. Journal of Bioscience and Bioengineering 101, 87–96. DOI: 10.1263/jbb.101.87
Sweetman J, Dimitroglou A, Davies S & Torrecillas S (2008) Gut morphology: a key to efficient nutrition. International Aquafeed 11, 26–30.
Tchorbanov B & Bozhkova M (1988) Enzymatic hydrolysis of cell protein in green algae Chlorella and Scenedesmus after extraction with organic solvents. Enzyme Microbiology Technology 10, 233–238. DOI: 10.1016/0141-0229(88)90072-5
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. DOI: 10.1016/j.aquaculture.2013.02.009
Teuling E, Wierenga PA, Agboola JO, Gruppen H & Schrama JW (2019) Cell wall disruption increases bioavailability of Nannochloropsis gaditana nutrients for juvenile Nile tilapia (Oreochromis niloticus). Aquaculture 499, 269–282. DOI: 10.1016/j.aquaculture.2018.09.047
Tibaldi E, Chini Zittelli G, Parisi G, Bruno M, Giorgi G, Tulli F, Venturini S, Tredici MR & Poli BM (2015) Growth performance and quality traits of European seabass (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. DOI: 10.1016/j.aquaculture.2015.02.002
Tibbetts SM, Milley JE & Lall SP (2015) Chemical composition and nutritional properties of freshwater and marine microalgal biomass cultured in photobioreactors. Journal of Applied Phycology 27, 1109–1119. DOI: 10.1007/s10811-014-0428-x
Tibbetts SM, MacPherson T, McGinn PJ & Fredeen AH (2016) In vitro digestion of microalgal biomass from freshwater species isolated in Alberta, Canada for monogastric and ruminant animal feed applications. Algal Research 19, 324–332. DOI: 10.1016/j.algal.2016.01.016
Tibbetts SM, Yasumaru F & Lemos D (2017) In vitro prediction of digestible protein content of marine microalgae (Nannochloropsis granulata) meals for Pacific white shrimp (Litopenaeus vannamei) and rainbow trout (Oncorhynchus mykiss). Algal Research 21, 76-80. DOI: 10.1016/j.algal.2016.11.010
Tibbetts SM (2018) The potential for ‘next-generation’, microalgae-based feed ingredients for salmonid aquaculture in context of the blue revolution. In Microalgal Biotechnology (pp. 151-175). IntechOpen. DOI: 10.5772/intechopen.73551
Tolasa S, Cakli S & Ostermeyer U (2005) Determination of astaxanthin and canthaxanthin in salmonid. European Food Research and Technology 221(6), 787–791. DOI: 10.1007/s00217-005-0071-5
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. Journal of Aquatic Food Product Technology 21, 188–197. DOI: 10.1080/10498850.2012.664803
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 Physiology and Biochemistry 45(3), 1067–1081. DOI: 10.1007/s10695-019-00621-w
Valente LMP, Gouveia A, Rema P, Matos J, Gomes EF & Pinto IS (2006) Evaluation of three seaweeds Gracilaria bursa-pastoris, Ulva rigida and Gracilaria cornea as dietary ingredients in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture 252, 85–91. DOI: 10.1016/j.aquaculture.2005.11.052
Venkataraman LV & Becker EW (1985) Biotechnology and utilization of algae: the Indian experience. Department of Science & Technology and Central Food Technological Research Institute, Mysore, India.
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. DOI: 10.1016/j.aquaculture.2014.05.010
Vizcaíno AJ, Mendes SI, Varela JL, Ruiz‐Jarabo I, Rico R, Figueroa FL, Abdala R, Moriñigo MA, Mancera JM & Alarcón FJ (2016a) Growth, tissue metabolites and digestive functionality in Sparus aurata juveniles fed different levels of macroalgae, Gracilaria cornea and Ulva rigida. Aquaculture Research 47(10), 3224–3238. DOI: 10.1111/are.12774
Vizcaíno AJ, Saéz MI, López G, Arizcun M, Abellán E, Martínez TF & Alarcón FJ (2016b) Tetraselmis suecia and Tisochrysis lutea meal as dietary ingredients for gilthead seabream (Sparus aurata L.) fry. Journal of Applied Phycology 28(5), 2843–2855. DOI: 10.1007/s10811-016-0845-0
Vizcaíno AJ, Rodiles A, López G, Sáez MI, Herrera M, Hachero I, Martínez TF, Cerón-García MC & Alarcón FJ (2018) Growth performance, body composition, and digestive functionality of Senegalese sole (Solea senegalensis Kaup, 1858) juveniles fed diets including microalgae freeze-dried biomass. Fish Physiology and Biochemistry 44(2), 661–677. DOI: 10.1007/s10695-018-0462-8
Vizcaíno AJ, Fumanal M, Sáez MI, Martínez TF, Moriñigo MA, Fernández-Díaz, C, Anguís V, Balebona MC & Alarcón FJ (2019a) Evaluation of Ulva ohnoi as functional dietary ingredient in juvenile Senegalese sole (Solea senegalensis): Effects on the structure and functionality of the intestinal mucosa. Algal Research 42, 101608. DOI: 10.1016/j.algal.2019.101608
Vizcaíno AJ, Sáez MI, Martínez TF, Acién FG & Alarcón FJ (2019b) Differential hydrolysis of proteins of four microalgae by the digestive enzymes of gilthead sea bream and Senegalese sole. Algal Research 37, 145–153. DOI: 10.1016/j.algal.2018.11.018
Vizcaíno AJ, Galafat A, Sáez MI, Martínez TF & Alarcón FJ (2020) Partial characterization of protease inhibitors of Ulva ohnoi and their effect on digestive proteases of marine fish. Marine Drugs 18(6), 319. DOI: 10.3390/md18060319
Volkman JK, Jeffrey SW, Nichols PD, Rogers GI & Garland CD (1989) Fatty acid and lipid composition of 10 species of microalgae used in aquiculture. Journal of Experimental Marine Biology and Ecology 128(3), 219-240. DOI: 10.1016/0022-0981(89)90029-4
Walker AB & Berlinsky DL (2011) Effects of partial replacement of fishmeal protein by microalgae on growth, feed intake, and body composition of Atlantic cod. North American Journal of Aquaculture 73, 76–83. DOI: 10.1080/15222055.2010.549030
Wan AHL, Simon JD, Soler-Vila A, Fitzgerald R & Johnson MP (2019) Macroalgae as a sustainable aquafeed ingredient. Reviews in Aquaculture 11(3), 458–492. DOI: 10.1111/raq.12241
Wang C, Hu W, Wang L, Qiao H, Wu H & Xu Z (2019) Effects of dietary supplementation with Sargassum horneri meal on growth performance, body composition, and immune response of juvenile turbot. Journal of Applied Phycology 31(1), 771–778. DOI: 10.1007/s10811-018-1590-3
Wilson RP (2003) Amino acids and proteins. In Fish Nutrition (pp. 143-179). Academic Press.
Xu S, Zhang L, Wu Q, Liu X, Wang S, You C & Li Y (2011) Evaluation of dried seaweed Gracilaria lemaneiformis as an ingredient in diets for teleost fish Siganus canaliculatus. Aquaculture International 19, 1007–1018. DOI: 10.1007/s10499-011-9418-z
Yadav G, Meena DK, Sahoo AK, Das BK & Sen R (2020) Effective valorization of microalgal biomass for the production of nutritional fish-feed supplements. Journal of Cleaner Production 243, 118697. DOI: 10.1016/j.jclepro.2019.118697
Yarnold J, Karan H, Oey M & Hankamer B (2019) Microalgal aquafeeds as part of a circular bioeconomy. Trends in Plant Science 24(10), 959–970. DOI: 10.1016/j.tplants.2019.06.005
