Skip to main content

Advertisement

Log in

Exploring the potential of seaweed Gracilaria gracilis and microalga Nannochloropsis oceanica, single or blended, as natural dietary ingredients for European seabass Dicentrarchus labrax

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Gracilaria gracilis and Nannochloropsis oceanica, single or blended, were tested in European seabass (Dicentrarchus labrax) diets. A control (CTRL) diet was compared with experimental diets including either 8% G. gracilis (GRA8), 8% N. oceanica (NAN8), or a blend of 4% of each alga (NAN4GRA4). After 106 days of feeding, growth, nutrient utilization, antioxidant defense, immunological status, and end-product quality were evaluated. All fish exhibited similar feed intake (1.4–1.5%), body weight, growth, and feed conversion ratio (1.6). Dietary inclusion N. oceanica did not affect digestible N intake and gain. Fish fed GRA8 had the lowest digestible N and energy intake (P < 0.05), and simultaneously the highest nitrogen retention efficiency and energy retention efficiency, resulting in a N and energy gain similar to all other treatments. All fish had well-preserved intestinal morphology; feeding NAN8 resulted in a significant increase in neutral goblet cells compared with GRA8. Fish fed the algal diets had significantly lower (P < 0.05) hepatosomatic index (1.7–1.8 vs 2.1) and plasma triglyceride levels than CTRL, but whole body composition remained similar among treatments. The liver total antioxidant capacity of fish fed NAN8 was significantly higher than that of fish fed GRA8 but did not differ significantly from the CTRL group. NAN4GRA4 resulted in lower values of total glutathione, glutathione peroxidase, and alternative complement. N. oceanica decreased fillet springiness; however, with NAN4GRA4, the muscle fillet became less resilient. G. gracilis and N. oceanica biomass, either used single (8%) or blended (4% each), can be valuable natural ingredients for partial replacement of fish meal in European seabass diets.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aaslyng MD, Bejerholm C, Ertbjerg P, Bertram HC, Andersen HJ (2003) Cooking loss and juiciness of pork in relation to raw meat quality and cooking procedure. Food Qual Prefer 14:277–288

    Google Scholar 

  • Abreu MH, Pereira R, Yarish C, Buschmann AH, Sousa-Pinto I (2011) IMTA with Gracilaria vermiculophylla: productivity and nutrient removal performance of the seaweed in a land-based pilot scale system. Aquaculture 312:77–87

    Google Scholar 

  • AFNOR (1992) Viandes, préparations de viande et produits à base de viande - Détermination de la teneur en phosphore total. NF:V04–V406

  • Angell AR, Angell SF, de Nys R, Paul NA (2016) Seaweed as a protein source for mono-gastric livestock. Trends Food Sci Technol 54:74–84

    CAS  Google Scholar 

  • AOAC (2006) Official methods of analysis of AOAC International, 18th edn. AOAC International, Maryland

    Google Scholar 

  • Araújo M, Rema P, Sousa-Pinto I, Cunha LM, Peixoto MJ, Pires MA, Seixas F, Brotas V, Beltrán C, Valente LMP (2016) Dietary inclusion of IMTA-cultivated Gracilaria vermiculophylla in rainbow trout (Oncorhynchus mykiss) diets: effects on growth, intestinal morphology, tissue pigmentation, and immunological response. J Appl Phycol 28:679–689

    Google Scholar 

  • Archibeque S, Ettinger A, Willson B (2009) Nannochloropsis oculata as a source for animal feed. Acta Agro Hung 57:245–248

    CAS  Google Scholar 

  • Ashour M, Elshobary ME, El-Shenody R, Kamil A-W, Abomohra AE-F (2019) Evaluation of a native oleaginous marine microalga Nannochloropsis oceanica for dual use in biodiesel production and aquaculture feed. Biomass Bioenergy 120:439–447

    CAS  Google Scholar 

  • Aussanasuwannakul A, Slider SD, Salem M, Yao J, Brett Kenney P (2012) Comparison of variable-blade to Allo-Kramer shear method in assessing rainbow trout (Oncorhynchus mykiss) fillet firmness. J Food Sci 77:S335–S341

    CAS  PubMed  Google Scholar 

  • Baker MA, Cerniglia GJ, Zaman A (1990) Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples. Anal Biochem 190:360–365

    CAS  PubMed  Google Scholar 

  • Bates JM, Akerlund J, Mittge E, Guillemin K (2007) Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in Zebrafish in response to the gut microbiota. Cell Host Microbe 6:371–382

    Google Scholar 

  • Batista S, Medina A, Pires MA, Moriñigo MA, Sansuwan K, Fernandes JMO, Valente LMP, Ozório ROA (2016) Innate immune response, intestinal morphology and microbiota changes in Senegalese sole fed plant protein diets with probiotics or autolyzed yeast. Appl Microbiol Biot

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

    CAS  Google Scholar 

  • Belal E, Khalafalla M, El-hais AMA (2012) Use of spirulina (Arthrospira fusiformis) for promoting growth of Nile Tilapia fingerlings. Afr J Microbiol Res 6

  • Bellou S, Baeshen MN, Elazzazy AM, Aggeli D, Sayegh F, Aggelis G (2014) Microalgal lipids biochemistry and biotechnological perspectives. Biotech Adv 32:1476–1493

    CAS  Google Scholar 

  • Bernstein AM, Ding EL, Willett WC, Rimm EB (2012) A meta-analysis shows that docosahexaenoic acid from algal ail reduces serum triglycerides and increases HDL-cholesterol and LDL-cholesterol in persons without coronary heart disease. J Nutr 142:99–104

    CAS  PubMed  Google Scholar 

  • Biller JD, Takahashi LS (2018) Oxidative stress and fish immune system: phagocytosis and leukocyte respiratory burst activity. An Acad Bras Cienc 90:3403–3414

    CAS  PubMed  Google Scholar 

  • Bird RP, Draper HH (1984) Comparative studies on different methods of malonaldehyde determination. Meth Enzymol 105: 299–305.

  • Bolin DW, King RP, Klosterman EW (1952) A simplified method for the determination of chromic oxide (Cr2O3) when used as an index substance. Science 116:634–635

    CAS  PubMed  Google Scholar 

  • Borges P, Oliveira B, Casal S, Dias J, Conceição L, Valente LMP (2009) Dietary lipid level affects growth performance and nutrient utilisation of Senegalese sole (Solea senegalensis) juveniles. Brit J Nutr 102:1007–1014

    CAS  PubMed  Google Scholar 

  • Boshra H, Li J, Sunyer JO (2006) Recent advances on the complement system of teleost fish. Fish Shellfish Immun 20:239–262

    CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  Google Scholar 

  • Cheng J-H, Sun D-W, Han Z, Zeng X-A (2014) Texture and structure measurements and analyses for evaluation of fish and fillet freshness quality: a review. Compr Rev Food Sci Food Saf 13:52–61

    Google Scholar 

  • Cho CY, Slinger SJ (1979) Apparent digestibility measurement in feedstuffs for rainbow trout. In: Halver JE, Tiews K (eds) Finfish nutrition and fish feed technology, vol 2. Heenemann, Berlin, pp 239–247

    Google Scholar 

  • Choubert G, Blanc JM, Vallée F (1997) Colour measurement, using the CIELCH colour space, of muscle of rainbow trout, Oncorhynchus mykiss (Walbaum), fed astaxanthin: effects of family, ploidy, sex, and location of reading. Aquac Res 28:15–22

    Google Scholar 

  • Claiborne A (1985) Catalase activity. In: Greenwald R (ed) CRC handbook of methods in oxygen radical research. CRC Press, Boca Raton, pp 283–284

    Google Scholar 

  • Costas B, Conceição LEC, Aragão C, Martos JA, Ruiz-Jarabo I, Mancera JM, Afonso A (2011) Physiological responses of Senegalese sole (Solea senegalensis Kaup, 1858) after stress challenge: effects on non-specific immune parameters, plasma free amino acids and energy metabolism. Aquaculture 316:68–76

    CAS  Google Scholar 

  • Coz-Rakovac R, Strunjak-Perovic I, Hacmanjek M, Topic Popovic N, Lipej Z, Sostaric B (2005) Blood chemistry and histological properties of wild and cultured sea bass (Dicentrarchus labrax) in the North Adriatic Sea. Vet Res Commun 29:677–687

    CAS  PubMed  Google Scholar 

  • Deplancke B, Gaskins HR (2001) Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am J Clin Nutr 73:1131S–1141S

    CAS  PubMed  Google Scholar 

  • Ellis AE (1990) Lysozyme assays. In: FT SJS, Anderson DP, Roberson BS, van Muiswinkel WB (eds) Techniques in fish immunology. SOS Publications, Fair Haven, pp 101–103

    Google Scholar 

  • Galeano J, Lopez-Herrera A, Suescún J (2015) The probiotic Enterococcus faecium modifies the intestinal morphometric parameters in weaning piglets. Rev Fac Nac Agro 69:7803–7811

    Google Scholar 

  • Gatlin DM, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl Å, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquac Res 38:551–579

    CAS  Google Scholar 

  • Gong Y, Sørensen SL, Dahle D, Nadanasabesan N, Dias J, Valente LMP, Sørensen M, Kiron V (2020) Approaches to improve utilization of Nannochloropsis oceanica in plant-based feeds for Atlantic salmon. Aquaculture. https://doi.org/10.1016/j.aquaculture.2020.735122:735122

  • Grau A, Crespo S, Sarasquete MC, de Canales MLG (1992) The digestive tract of the amberjack Seriola dumerili, Risso: a light and scanning electron microscope study. J Fish Biol 41:287–303

    CAS  Google Scholar 

  • Guerreiro I, Magalhães R, Coutinho F, Couto A, Sousa S, Delerue-Matos C, Domingues VF, Oliva-Teles A, Peres H (2019) Evaluation of the seaweeds Chondrus crispus and Ulva lactuca as functional ingredients in gilthead seabream (Sparus aurata). J Appl Phycol 31:2115–2124

    CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  PubMed  Google Scholar 

  • Harpaz S, Uni Z (1999) Activity of intestinal mucosal brush border membrane enzymes in relation to the feeding habits of three aquaculture fish species. Comp Biochem Physiol A 124:155-160

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

    Google Scholar 

  • Hinnebusch BF, Siddique A, Henderson JW, Malo MS, Zhang W, Athaide CP, Abedrapo MA, Chen X, Yang VW, Hodin RA (2004) Enterocyte differentiation marker intestinal alkaline phosphatase is a target gene of the gut-enriched Krüppel-like factor. Am J Physiol - Gastro L 286:G23–G30

    CAS  Google Scholar 

  • Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597

    CAS  Google Scholar 

  • Hoseinifar SH, Yousefi S, Capillo G, Paknejad H, Khalili M, Tabarraei A, Van Doan H, Spano N, Faggio C (2018) Mucosal immune parameters, immune and antioxidant defence related genes expression and growth performance of zebrafish (Danio rerio) fed on Gracilaria gracilis powder. Fish Shellfish Immunol 83:232–237

    CAS  PubMed  Google Scholar 

  • Husni A, Ustadi U, Wijaya H (2013) The use of Gracilaria sp. extract on refrigerated red tilapia fillet. J Biol Sci 13:640–644

    Google Scholar 

  • Hutchinson TH, Manning MJ (1996) Seasonal trends in serum lysozyme activity and total protein concentration in dab (Limanda limanda L.) sampled from Lyme Bay, U.K. Fish Shellfish Immun 6:473–482

    Google Scholar 

  • Jonsson, Sigurgisladottir S, Hafsteinsson, Kristbergsson K (2001) Texture properties of raw Atlantic salmon (Salmo salar) fillets measured by different methods in comparison to expressible moisture. Aquac Nutr 7:81–89

    Google Scholar 

  • Kim JJ, Khan WI (2013) Goblet cells and mucins: role in innate defense in enteric infections. Pathogens 2:55–70

    PubMed  PubMed Central  Google Scholar 

  • 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. Aquac Nut 18:521–531

    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

  • Lee J-C, Hou M-F, Huang H-W, Chang F-R, Chi-Chen Y, Tang J-Y, Chang H-W (2013) Marine algal natural products with anti-oxidative, anti-inflammatory, and anti-cancer properties. Cancer Cell Int 13:55

    PubMed  PubMed Central  Google Scholar 

  • Lu SC (2009) Regulation of glutathione synthesis. Mol Asp Med 30:42–59

    CAS  Google Scholar 

  • Magnoni LJ, Martos-Sitcha JA, Queiroz A, Calduch-Giner JA, Goncalves JFM, Rocha CMR, Abreu HT, Schrama JW, Ozorio ROA, Perez-Sanchez J (2017) Dietary supplementation of heat-treated Gracilaria and Ulva seaweeds enhanced acute hypoxia tolerance in gilthead sea bream (Sparus aurata). Biol Open 6:897–908

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maynard LA, Loosli JK, Hintz HF, Warner RG (1979) Animal nutrition. 7th edn., New York

  • Messina M, Bulfon C, Beraldo P, Tibaldi E, Cardinaletti G (2019) Intestinal morpho-physiology and innate immune status of European sea bass (Dicentrarchus labrax) in response to diets including a blend of two marine microalgae, Tisochrysis lutea and Tetraselmis suecica. Aquaculture 500:660–669

    CAS  Google Scholar 

  • Mohamed S, Hashim SN, Rahman HA (2012) Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends Food Sci Technol 23:83–96

    CAS  Google Scholar 

  • Mohandas J, Marshall JJ, Duggin GG, Horvath JS, Tiller DJ (1984) Low activities of glutathione-related enzymes as factors in the genesis of urinary bladder cancer. Cancer Res 44:5086–5091

    CAS  PubMed  Google Scholar 

  • 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. Int J Environ Res Public Health 15:E2436

  • Moreda-Piñeiro A, Peña-Vázquez E, Bermejo-Barrera P (2012) Significance of the presence of trace and ultratrace elements in seaweeds. In: Kim SK (ed) Handbook of marine macroalgae: biotechnology and applied phycology. John Wiley & Sons, Chichester, pp 116–170

    Google Scholar 

  • Moutinho S, Linares F, Rodríguez JL, Sousa V, Valente LMP (2018) Inclusion of 10% seaweed meal in diets for juvenile and on-growing life stages of Senegalese sole (Solea senegalensis). J Appl Phycol 30:3589–3601

    CAS  Google Scholar 

  • Mustafa MG, Umino T, Nakagawa H (1997) Limited synergistic effect of dietary Spirulina on vitamin C nutrition of red sea bream Pagrus major. J Mar Biotechnol 5:129–132

    CAS  Google Scholar 

  • Nakagawa H, Montgomery L (2007) Algae. In: Nakagawa H, Sato M, Gatlin D III (eds) Dietary supplements for the health and quality of cultured fish. CABI, pp 133–167

  • Nakagawa H, Mustafa MG, Takii K, Umino T, Kumai H (2000) Effect of dietary catechin and Spirulina on vitamin C metabolism in red sea bream. Fish Sci 66:321–326

    CAS  Google Scholar 

  • Natrah FMI, Yusoff F, Shariff M, Abas F, Mariana NS (2007) Screening of Malaysian indigenous microalgae for antioxidant properties and nutritional value. J Appl Phycol 19:711–718

    CAS  Google Scholar 

  • NRC (2011) Nutrient requirements of fish and shrimp. The National Academies Press

  • Patterson D, Gatlin DM (2013) Evaluation of whole and lipid-extracted algae meals in the diets of juvenile red drum (Sciaenops ocellatus). Aquaculture 416-417:92–98

    CAS  Google Scholar 

  • Peixoto MJ, Salas-Leitón E, Pereira LF, Queiroz A, Magalhães F, Pereira R, Abreu H, Reis PA, Gonçalves JFM, Ozório ROA (2016a) Role of dietary seaweed supplementation on growth performance, digestive capacity and immune and stress responsiveness in European seabass (Dicentrarchus labrax). Aquac Rep 3:189–197

    Google Scholar 

  • Peixoto MJ, Svendsen JC, Malte H, Pereira LF, Carvalho P, Pereira R, Gonçalves JFM, Ozório ROA (2016b) Diets supplemented with seaweed affect metabolic rate, innate immune, and antioxidant responses, but not individual growth rate in European seabass (Dicentrarchus labrax). J Appl Phycol 28:2061–2071

    CAS  Google Scholar 

  • Peixoto M, Magnoni L, Gonçalves JFM, Twijnstra RH, Kijjoa A, Pereira R, Palstra AP, Ozorio R (2018) Effects of dietary supplementation of Gracilaria sp. extracts on fillet quality, oxidative stress, and immune responses in European seabass (Dicentrarchus labrax). J Appl Phycol 31:761–770

    Google Scholar 

  • Peixoto MJ, Ferraz R, Magnoni LJ, Pereira R, Gonçalves JF, Calduch-Giner J, Pérez-Sánchez J, Ozório ROA (2019) Protective effects of seaweed supplemented diet on antioxidant and immune responses in European seabass (Dicentrarchus labrax) subjected to bacterial infection. Sci Rep 9:16134

    PubMed  PubMed Central  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. Aquac Nutr 20:646–653

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Quade MJ, Roth JA (1997) A rapid, direct assay to measure degranulation of bovine neutrophil primary granules. Vet Immunol Immunopathol 58:239–248

    CAS  PubMed  Google Scholar 

  • Radha P (2018) Proximate analysis and mineral composition of seaweeds of Manamelkudi Coast, Pudukkottai District, India. Int J Curr Microbiol App Sci 7:3121–3128

    CAS  Google Scholar 

  • 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 Aquac Soc 48:103–112

    CAS  Google Scholar 

  • Rajapakse N, Kim S-K (2011) Chapter 2 - nutritional and digestive health benefits of seaweed. In: Kim S-K (ed) Advances in food and nutrition research. Academic Press, pp 17–28

  • Ramos MA, Batista S, Pires MA, Silva AP, Pereira LF, Saavedra MJ, Ozorio ROA, Rema P (2017) Dietary probiotic supplementation improves growth and the intestinal morphology of Nile tilapia. Animal 11:1259–1269

    CAS  PubMed  Google Scholar 

  • Reka P, Azeez T, Seethalakshmi M (2017) Elemental composition of selected edible seaweeds using SEM- energy dispersive spectroscopic analysis. Int Food Res J 24:600–606

    CAS  Google Scholar 

  • Robertson JB, Van Soest PJ (1981) The detergent system of analysis and its application to human foods. In: James WPT, Olof T (eds) The analysis of dietary fiber in food. Marcel Dekker Inc., New York, pp 123–158

    Google Scholar 

  • Sabeena Farvin KH, Baron CP, Nielsen NS, Otte J, Jacobsen C (2010) Antioxidant activity of yoghurt peptides: part 2 – characterisation of peptide fractions. Food Chem 123:1090–1097

    CAS  Google Scholar 

  • 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. Aquac Nutr 22:109–119

    CAS  Google Scholar 

  • Schubert N, Garcia-Mendoza E, Pacheco-Ruiz I (2006) Carotenoid composition of marine red algae. J Phycol 42:1208–1216

    CAS  Google Scholar 

  • Sheikhzadeh N, Heidarieh M, Karimi Pashaki A, Nofouzi K, Ahrab Farshbafi M, Akbari M (2012) Hilyses®, fermented Saccharomyces cerevisiae, enhances the growth performance and skin non-specific immune parameters in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 32:1083–1087

    CAS  PubMed  Google Scholar 

  • 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. J Appl Phycol 27:1671–1680

    CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • Sotoudeh E, Mardani F (2018) Antioxidant-related parameters, digestive enzyme activity and intestinal morphology in rainbow trout (Oncorhynchus mykiss) fry fed graded levels of red seaweed, Gracilaria pygmaea. Aquac Nutr 24:777–785

    CAS  Google Scholar 

  • Specian RD, Oliver MG (1991) Functional biology of intestinal goblet cells. Am J Phys 260:C183–C193

    CAS  Google Scholar 

  • Spence C, Levitan C, Shankar M, Zampini M (2010) Does food color influence taste and flavor perception in humans? Chemos Percept 3:68–84

    Google Scholar 

  • Stadtlander T, Khalil WKB, Focken U, Becker K (2013) Effects of low and medium levels of red alga Nori (Porphyra yezoensis Ueda) in the diets on growth, feed utilization and metabolism in intensively fed Nile tilapia, Oreochromis niloticus (L.). Aquac Nutr 19:64–73

    CAS  Google Scholar 

  • Sunyer J, Tort L (1995) Natural hemolytic and bactericidal activities of sea bream Sparus aurata serum are effected by the alternative complement pathway. Vet Immunol Immun 45:333–345

    CAS  Google Scholar 

  • Teimouri M, Yeganeh S, Mianji GR, Najafi M, Mahjoub S (2019) The effect of Spirulina platensis meal on antioxidant gene expression, total antioxidant capacity, and lipid peroxidation of rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 45:977–986

    CAS  PubMed  Google Scholar 

  • Tibaldi E, Hakim Y, Uni Z, Tulli F, de Francesco M, Luzzana U, Harpaz S (2006) Effects of the partial substitution of dietary fish meal by differently processed soybean meals on growth performance, nutrient digestibility and activity of intestinal brush border enzymes in the European sea bass (Dicentrarchus labrax). Aquaculture 261:182–193

    CAS  Google Scholar 

  • 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 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

    CAS  Google Scholar 

  • Tibbetts S (2018) The potential for ‘next-generation’, microalgae-based feed ingredients for salmonid aquaculture in context of the blue revolution. In: Jacob-Lopes E, Zepka LQ, Queiroz MI (eds) Microalgal Biotechnology. Intechopen, Riejeka, pp 151–175

    Google Scholar 

  • Torres MD, Florez-Fernandez N, Dominguez H (2019) Integral utilization of red seaweed for bioactive production. Mar Drugs 17:e314

    PubMed  Google Scholar 

  • 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 Technol 21:188–197

    Google Scholar 

  • USEPA (1995) EPA method 3051: microwave assisted acid digestion of sediments, sludges, soils, and oils. Test methods for evaluating solid waste, 3rd edn. USEPA, Washington, D.C

    Google Scholar 

  • 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

    Google Scholar 

  • Valente LMP, Rema P, Ferraro V, Pintado M, Sousa-Pinto I, Cunha LM, Oliveira MB, Araújo M (2015) Iodine enrichment of rainbow trout flesh by dietary supplementation with the red seaweed Gracilaria vermiculophylla. Aquaculture 446:132–139

    CAS  Google Scholar 

  • Valente L, 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

    CAS  PubMed  Google Scholar 

  • Van Soest PJ, Robertson JB (1985) Analysis of forages and fibrous foods a laboratory manual for animal science. Department of Animal Science, Ithaca

    Google Scholar 

  • Varghese T, Mathew S (2017) Assessment of the textural variation of iced stored Anabas testudineus (Bloch, 1792) muscle tissue with emphasis on their collagen and myofibrillar protein content. J Food Sci Technol 54:2512–2518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vizcaíno AJ, Mendes SI, Varela JL, Ruiz-Jarabo I, Rico R, Figueroa FL, Abdala R, Moriñigo MÁ, Mancera JM, Alarcón FJ (2016) Growth, tissue metabolites and digestive functionality in Sparus aurata juveniles fed different levels of macroalgae, Gracilaria cornea and Ulva rigida. Aquac Res 47:3224–3238

    Google Scholar 

  • Vizcaíno A, Rodiles A, López G, Saez M, Herrera M, Hachero-Cruzado I, Martínez Moya T, Cerón-García MC, Alarcón F (2018) Growth performance, body composition, and digestive functionality of Senegalese sole (Solea senegalensis Kaup, 1858) juveniles fed diets including microalgae freeze-dried biomass. Fish Physiol Biochem 44

  • 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 Aquac 73:76–83

    Google Scholar 

  • Younis E-SM, Al-Quffail AS, Al-Asgah NA, Abdel-Warith A-WA, Al-Hafedh YS (2018) Effect of dietary fish meal replacement by red algae, Gracilaria arcuata, on growth performance and body composition of Nile tilapia Oreochromis niloticus. Saudi J Biol Sci 25:198–203

    CAS  PubMed  Google Scholar 

  • Zheng L-X, Chen X-Q, Cheong K-L (2020) Current trends in marine algae polysaccharides: the digestive tract, microbial catabolism, and prebiotic potential. Int J Biol Macromol 151:344–354

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Work supported by Project “MARINALGAE4AQUA - Improving bio-utilisation of marine algae as sustainable feed ingredients to increase efficiency and quality of aquaculture production”, financed by FCT-Portugal through the research project ERA-NET COFASP/004/2015. The authors thank Tiago Sá, Catarina Ribeiro, Alexandra Marques, and Marianna Dourou for their technical support during the feeding trial chemical and chemical analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luisa M. P. Valente.

Ethics declarations

The present study was performed by accredited scientists, in compliance with the guidelines of the European Union (directive 2010/63/EU) and Portuguese law (Decreto-Lei no. 113/2013, de 7 de Agosto) on the protection of animals used for scientific purposes. All animal procedures were subject to an ethical review process carried out by CIIMAR animal welfare body (ORBEA-CIIMAR) and further approved by national competent authorities.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Batista, S., Pereira, R., Oliveira, B. et al. Exploring the potential of seaweed Gracilaria gracilis and microalga Nannochloropsis oceanica, single or blended, as natural dietary ingredients for European seabass Dicentrarchus labrax. J Appl Phycol 32, 2041–2059 (2020). https://doi.org/10.1007/s10811-020-02118-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-020-02118-z

Keywords

Navigation