Comparison of β-carotene and Spirulina (Arthrospira platensis) in mullet (Mugil liza) diets and effects on antioxidant performance and fillet colouration

  • Victor Torres Rosas
  • José María Monserrat
  • Martin Bessonart
  • Larisa Magnone
  • Luis Alberto Romano
  • Marcelo Borges TesserEmail author


The addition of pure carotenoids is a common practice in some aquaculture species production since its use in fish feed is known to improve carcass and antioxidant capacity. Spirulina (Arthrospira) cyanobacteria are a rich source of carotenoids that has proven health benefits for fish welfare. In the current experiment, four isonitrogenous (38%) isolipidic (9%) diets were made, including a control diet (free of β-carotene and Spirulina, SP0), β-carotene diet (50 mg kg−1, β0), and two Spirulina (Arthrospira platensis) diets with 2% (SP2) and 4% (SP4) of total feed inclusion. The experimental diets were given to juvenile mullets in a controlled recirculation system. The parameters evaluated were growth, colour, total carotene content of muscle, and antioxidant capacity of the liver and muscle. Significant differences were found (p < 0.05) in the final weight, specific growth rate, and feed conversion ratio between the SP0 treatment and the β0, SP2, and SP4 treatments. The colorimetric analysis showed that the redness and carotene deposition in muscle of mullet is statistically the same between β0 and SP4. Mullets fed with Spirulina (SP2 and SP4 treatments) had a statistical higher antioxidant capacity against radical peroxyls in liver tissue, showing lower lipid peroxidation (TBARS). In conclusion, Spirulina can be a suitable substitute for pure β-carotene addition in fish diets, improving some of the health benefits from this carotene.


Antioxidant capacity Colorimetric analysis Fish TBARS 


Funding information

Part of this study was supported by a grant from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq–Universal, process number 404075/2016-9 and CNPq, process number 408921/2013-7- Prospecção de 245 substâncias antioxidantes de organismos marinhos–SAOMAR) and by Capes (Ciências do Mar). Monserrat, J.M., Romano, L.A., and Tesser, M.B. are research fellows from the Brazilian agency CNPq.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All experimental procedures involving fish were performed in accordance with the guidelines and approved by the Ethics Committee (FURG- CEUA Pq036/2014).


  1. Abdel-Tawwab M, Ahmad M (2009) Live Spirulina (Arthrospira platensis) as a growth and immunity promoter for Nile tilapia, (Oreochromis niloticus L.), challenged with pathogenic Aeromonas hydrophila. Aquac Res 40:1037–1046CrossRefGoogle Scholar
  2. Adel M, Yeganeh S, Dadar M, Sakai M, Dawood MAO (2016) Effects of dietary Spirulina platensis on growth performance, humoral and mucosal immune responses and disease resistance in juvenile great sturgeon (Huso huso Linnaeus, 1754). Fish Shellfish Immunol 56:436–444CrossRefGoogle Scholar
  3. Ahmed F, Fanning K, Netzel M, Turner W, Li Y, Schenk PM (2014) Profiling of carotenoids and antioxidant capacity of microalgae from subtropical coastal and brackish waters. Food Chem 165:300–306CrossRefGoogle Scholar
  4. Amado LL, Garcia ML, Ramos PB, Freitas RF, Zafalon B, Ferreira JL, Yunes JS, Monserrat JM (2009) A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Sci Total Environ 407:2115–2123CrossRefGoogle Scholar
  5. Amar EC, Kiron V, Satoh S, Watanabe T (2001) Influence of various dietary synthetic carotenoids on bio-defence mechanisms in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac Res 32:162–173CrossRefGoogle Scholar
  6. American Public Health Association (APHA) (2005) Standard methods for the examination of water and wastewater, 21st edn. APHA, WashingtonGoogle Scholar
  7. AOAC (Association of Official Analytical Chemists) (2000) Official methods of analysis of the AOAC, 16th edn. AOAC international, WashingtonGoogle Scholar
  8. Belay A (2002) The potential application of Spirulina (Arthrospira) as a nutritional and therapeutic supplement in health management. JANA 5:26–48Google Scholar
  9. Belay A (2008) Spirulina (Arthrospira): production and quality assurance. In: Gershwin ME, Belay A (eds) Spirulina in human nutrition and health. CRC Press, Boca Raton, pp 1–25Google Scholar
  10. Benderschneider K, Robinson RJ (1983) A new spectrophotometric method for determination of nitrate in seawater. J Mar Res 1:69–87Google Scholar
  11. Bermejo P, Piñero E, Villar ÁM (2008) Iron-chelating ability and antioxidant properties of phycocyanin isolated from a protean extract of Spirulina platensis. Food Chem 110:436–445CrossRefGoogle Scholar
  12. Biswal S (2014) Oxidative stress and astaxanthin: the novel supernutrient carotenoid. Inter J Health Allied Sci 3:147CrossRefGoogle Scholar
  13. Braz SR, Silva IO, Tesser MB, Sampaio LA, Rodrigues RV (2017) Benzocaína, MS-222, Eugenol e Mentol como anestésicos para juvenis de tainha Mugil liza. Bol Inst Pesca 43:605–613CrossRefGoogle Scholar
  14. Britton G (1995) Structure and properties of carotenoids in relation to function. FASEB J 9:1551–1558CrossRefGoogle Scholar
  15. Careri M, Furlattini L, Mangia A, Musc M, Anklam E, Theobald A, von Holst C (2001) Supercritical fluid extraction for liquid chromatographic determination of carotenoids in Spirulina pacifica algae: a chemometric approach. J Chromatogr A 912:61–71CrossRefGoogle Scholar
  16. Carvalho C, Bianchini A, Tesser MB, Sampaio LA (2010) The effect of protein levels on growth, postprandial excretion and tryptic activity of juvenile mullet Mugil platanus (Günther). Aquac Res 41:511–518CrossRefGoogle Scholar
  17. Chaiklahan R, Chirasuwan N, Bunnag B (2012) Stability of phycocyanin extracted from Spirulina sp.: influence of temperature, pH and preservatives. Process Biochem 47:659–664CrossRefGoogle Scholar
  18. Chen H-W, Yang T-S, Chen M-J, Chang Y-C, Wang EIC, Ho C-L, Lai Y-J, Yu C-C, Chou J-C, Chao LK-P, Liao P-C (2014) Purification and immunomodulating activity of C-phycocyanin from Spirulina platensis cultured using power plant flue gas. Process Biochem 49:1337–1344CrossRefGoogle Scholar
  19. Chew BP, Jean SP (2004) Carotenoid action on the immune response. J Nutr 134:257S–261SCrossRefGoogle Scholar
  20. Christiansen R, Struksnaes G, Estermann R, Torrissen OJ (1995) Assessment of flesh colour in Atlantic salmon, Salmo salar L. Aquac Res 26:311–321CrossRefGoogle Scholar
  21. Crosetti D (2016) Current state of grey mullet fisheries and culture. In: Crosetti D, Blaber S (eds) Biology, ecology and culture of Grey mullet (Mugilidae). CRC Press, Boca Raton, pp 398–450CrossRefGoogle Scholar
  22. EFSA (European Food Safety Authority) (2005) Opinion of the scientific panel on additives and products or substances used in animal feed on the request from the European commission on the safety of use of colouring agents in animal nutrition. Part I. General principles and astaxanthin. EFSA J 291:1–40Google Scholar
  23. Erdman JW, Bierer TL, Gugger ET (1993) Absorption and transport of carotenoids. Ann N Y Acad Sci 691:76–85CrossRefGoogle Scholar
  24. Estrada JP, Bescós PB, Del Fresno AV (2001) Antioxidant activity of different fractions of Spirulina platensis protean extract. Farmaco 56:497–500CrossRefGoogle Scholar
  25. FAO (2016) The state of world fisheries and aquaculture (2016). Contributing to food security and nutrition for all, RomeGoogle Scholar
  26. Gad AS, Khadrawy YA, El-Nekeety AA, Mohamed SR, Hassan NS, Abdel-Wahab MA (2011) Antioxidant activity and hepatoprotective effects of whey protein and Spirulina in rats. Nutrition 27:582–589CrossRefGoogle Scholar
  27. Galvão MSN, Fenerich-Verani N, Yamanaka N, Oliveira IR (1997) Histologia do sistema digestivo da tainha Mugil platanus Günther, 1880 (Osteichthyes, Mugilidae) durante as fases larval e juvenil. Bol Inst Pesca 24:91–100Google Scholar
  28. Godinho HM, Kavamoto ET, Talmelli EF et al (1993) Induced spawning of the mullet Mugil platanus Günther 1880 in Cananéia. São Paulo. Brazil. Bol Inst Pesca 20:59–66Google Scholar
  29. Habib MAB, Parvin M, Huntington TC, Hasan MR (2008) A review on culture, production and use of Spirulina as food for humans and feeds for domestic animals and fish. FAO Fisheries Circular 1304, Food and Agriculture Organization of the United Nations, Rome 41 ppGoogle Scholar
  30. Halliwell B (2007) Oxidative stress and cancer: have we moved forward. Biochem J 401:1–11CrossRefGoogle Scholar
  31. Hu CJ, Chen SM, Pan CH, Huang CH (2006) Effects of dietary vitamin A or β-carotene concentrations on growth of juvenile hybrid tilapia, Oreochromis niloticus× O. aureus. Aquaculture 253:602–607CrossRefGoogle Scholar
  32. Hunt RWG (1977) The specification of colour appearance: I. Concepts and terms. Color Res Appl 2:55–68CrossRefGoogle Scholar
  33. Kaisuyama M, Matsuno T (1988) Carotenoid and vitamin A, and metabolism of carotenoids, β-carotene, canthaxanthin, astaxanthin, zeaxanthin, lutein and tunaxanthin in tilapia Tilapia nilotica. Comp Biochem Physiol B 90:131–139CrossRefGoogle Scholar
  34. Khachik F, De Moura FF, Zhao DY, Aebischer CP, Bernstein PS (2002) Transformations of selected carotenoids in plasma, liver, and ocular tissues of humans and in nonprimate animal models. Invest Ophthalmol Vis Sci 43:3383–3392Google Scholar
  35. Kim MY, Cheong SH, Lee JH, Kim MJ, Sok DE, Kim MR (2010) Spirulina improves antioxidant status by reducing oxidative stress in rabbits fed a high-cholesterol diet. J Med Food 13:420–426CrossRefGoogle Scholar
  36. Kim SS, Rahimnejad S, Kim KW, Lee KJ (2013) Partial replacement of fish meal with Spirulina pacifica in diets for parrot fish (Oplegnathus fasciatus). Turk J Fish Aquat Sci 13:197–204Google Scholar
  37. Ma TS, Zuazago G (1942) Micro-Kjeldahl determination of nitrogen. A new indicator and an improved rapid method. Ind Eng Chem 14:280–282Google Scholar
  38. Maltez LC, Stringhetta GR, Enamorado AD, Okamoto MH, Romano LA, Monserrat JM, Sampaio LA, Garcia L (2017) Ammonia exposure and subsequent recovery trigger oxidative stress responses in juveniles of Brazilian flounder Paralichthys orbignyanus. Fish Physiol Biochem 43:1747–1759CrossRefGoogle Scholar
  39. Miki W, Yamaguchi K, Konosu S (1986) Chemistry and utilization of plankton. VIII. Carotenoid composition of Spirulina máxima. Bull Jpn Soc Sci Fish 52:1225–1227CrossRefGoogle Scholar
  40. Nagao A (2011) Absorption and metabolism of dietary carotenoids. Biofactors 37:83–87CrossRefGoogle Scholar
  41. Nickell DC, Bromage NR (1998) The effect of dietary lipid level on variation of flesh pigmentation in rainbow trout (Oncorhynchus mykiss). Aquaculture 161:237–251CrossRefGoogle Scholar
  42. Niu J, Wen H, Li CH (2014) Comparison effect of dietary astaxanthin and β-carotene in the presence and absence of cholesterol supplementation on growth performance, antioxidant capacity and gene expression of Penaeus monodon under normoxia and hypoxia condition. Aquaculture 422:8–17CrossRefGoogle Scholar
  43. NRC (National Research Council) (2011) Nutrient requirements of fish and shrimp. Animal Nutrition Series, National Academic Press, Washington, DC. 375 pGoogle Scholar
  44. Oakes KD, Van Der Kraak GJ (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat Toxicol 63:447–463CrossRefGoogle Scholar
  45. Oliva-Teles A (2012) Nutrition and health of aquaculture fish. J Fish Dis 35:83–108CrossRefGoogle Scholar
  46. Olson JA (1989) Provitamin A function of carotenoids: the conversion of beta-carotene into vitamin A. J Nutr 119:105–108CrossRefGoogle Scholar
  47. Pisoschi AM, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. Eur J Med Chem 97:55–74CrossRefGoogle Scholar
  48. Pohlenz C, Gatlin DM (2014) Interrelationships between fish nutrition and health. Aquaculture 431:111–117CrossRefGoogle Scholar
  49. Priyadarshani AMB (2017) A review on factors influencing bioaccessibility and bioefficacy of carotenoids. Crit Rev Food Sci Nutr 57:1710–1717CrossRefGoogle Scholar
  50. Promya J, Chitmanat C (2011) The effects of Spirulina platensis and Cladophora algae on the growth performance, meat quality and immunity stimulating capacity of the African sharptooth catfish (Clarias gariepinus). Int J Agric Biol 13:77–82Google Scholar
  51. Ramos LRV, Romano LA, Monserrat JM, Abreu PC, Verde PE, Tesser MB (2015) Biological responses in mullet Mugil liza juveniles fed with guar gum supplemented diets. Anim Feed Sci Technol 205:98–106CrossRefGoogle Scholar
  52. Ravi M, De SL, Azharuddin DS, Paul SFD (2010) The beneficial effects of Spirulina focusing on its immunomodulatory and antioxidant properties. Nutr Diet Suppl 2:73–83Google Scholar
  53. Sohn JH, Taki Y, Ushio H (2005) Lipid oxidations in ordinary and dark muscles of fish: influences on rancid off-odor development and color darkening of yellowtail flesh during ice storage. J Food Sci 70:s490–s496CrossRefGoogle Scholar
  54. Stahl W, Sies H (2003) Antioxidant activity of carotenoids. Mol Asp Med 24:345–351CrossRefGoogle Scholar
  55. Strickland JDH, Parsons TR (1972) A practical handbook for seawater analysis. Bull Fish Res Board Canada 167:1–310Google Scholar
  56. Teimouri M, Amirkolaie AK, Yeganeh S (2013a) The effects of Spirulina platensis meal as a feed supplement on growth performance and pigmentation of rainbow trout (Oncorhynchus mykiss). Aquaculture 396:14–19CrossRefGoogle Scholar
  57. Teimouri M, Amirkolaie AK, Yeganeh S (2013b) The effects of dietary supplement of Spirulina platensis on blood carotenoid concentration and fillet color stability in rainbow trout (Oncorhynchus mykiss). Aquaculture 414:224–228CrossRefGoogle Scholar
  58. Teimouri M, Yeganeh S, Amirkolaie AK (2016) The effects of Spirulina platensis meal on proximate composition, fatty acid profile and lipid peroxidation of rainbow trout (Oncorhynchus mykiss) muscle. Aquac Nutr 22:559–566CrossRefGoogle Scholar
  59. 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 2:106–110Google Scholar
  60. Torrissen OJ, Christiansen R (1995) Requirements for carotenoids in fish diets. J Appl Ichthyol 11:225–230CrossRefGoogle Scholar
  61. van Het Hof KH, West CE, Weststrate JA, Hautvast JG (2000) Dietary factors that affect the bioavailability of carotenoids. J Nutr 130:503–506CrossRefGoogle Scholar
  62. Yanar Y, Çelik M, Yanar M (2004) Seasonal changes in total carotenoid contents of wild marine shrimps (Penaeus semisulcatus and Metapenaeus monoceros) inhabiting the eastern Mediterranean. J Food Chem 88:267–269CrossRefGoogle Scholar
  63. Zamora-Sillero J, Ramos LRV, Romano LA, Monserrat JM, Tesser MB (2013) Effect of dietary dextrin levels on the growth performance, blood chemistry, body composition, hepatic triglicerides and glycogen of Lebranche mullet juveniles (Mugil liza Valenciennes 1836, Mugilidae). J Appl Ichthyol 29:1342–1347CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Instituto de Oceanografia (IO)EMA, Universidade Federal do Rio Grande-FURGRio GrandeBrazil
  2. 2.Laboratório de Nutrição de Organismos Aquáticos (LANOA), IORio GrandeBrazil
  3. 3.Instituto de Ciências Biológicas (ICB)Universidade Federal do Rio Grande–FURGRio GrandeBrazil
  4. 4.Laboratório de Bioquímica Funcional de Organismos Aquáticos (BIFOA), IORio GrandeBrazil
  5. 5.Laboratorio de Recursos Naturales Facultad de Ciencias–UDeLaRMontevideoUruguay
  6. 6.Estación Experimental de Investigaciones Marinas y Acuicultura, DINARACabo PolonioUruguay
  7. 7.Laboratório de Patologia e Imunologia de Organismos AquáticosInstituto de OceanografiaRio GrandeBrazil

Personalised recommendations