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Journal of Applied Phycology

, Volume 31, Issue 2, pp 1455–1465 | Cite as

Red seaweed Pyropia columbina as antioxidant supplement in feed for cultured juvenile Pacú (Piaractus mesopotamicus)

  • Raúl E. CianEmail author
  • Carla Bacchetta
  • Andrea Rossi
  • Jimena Cazenave
  • Silvina R. Drago
Article

Abstract

The aim of this study was to evaluate the antioxidant effect of red seaweed Pyropia columbina on juvenile Pacú (Piaractus mesopotamicus). Two hundred and ten (n = 210) fish were fed for 90 days with a control extruded feed (CEF) or the same feed added with P. columbina (35 g kg−1) (PcEF). No significant difference in final body weight, specific growth rate, condition factor, and liver somatic index was detected between dietary treatments (p > 0.05). Fish fed with PcEF showed lower lipid peroxidation (28.2 ± 2.9 vs. 39.4 ± 3.7 mmol malondialdehyde mg−1 protein) and superoxide dismutase (23.3 ± 2.3 vs. 37.7 ± 3.0 U mg−1 protein) and reduced SOD/CAT ratio (5.5 ± 0.3 vs. 8.1 ± 0.7) in intestine than those fed with CEF (p < 0.05). These results also were observed in liver and white muscle, indicating a systemic effect. No difference in glutathione S-transferase and catalase (CAT) activity in intestine, liver, and white muscle was detected between dietary treatments (p > 0.05). PcEF showed higher hemoglobin (7.5 ± 0.4 vs. 6.6 ± 0.3 g 100 mL−1) and mean corpuscular hemoglobin concentration (18.4 ± 1.8 vs. 25.7 ± 2.7%) than those fed with CEF diet (p < 0.05). Beneficial effects on lipid metabolism were observed in fish fed with PcEF respect to control diet. Pyropia columbina could be used as a natural antioxidant ingredient in fish feeding contributing a better nutritional status of cultured fish.

Keywords

In vivo antioxidant effect Red seaweed Piaractus mesopotamicus Extruded fish feed 

Notes

Acknowledgements

All authors read and approved the final manuscript.

Funding information

This work was funded by the projects PICT-2013-1804 and CAI + D 2011 PI 0292 LI from ANPCyT and Universidad Nacional del Litoral, respectively.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

References

  1. Aguilera J, Dummermuth A, Karsten U, Schriek R, Wiencke C (2002) Enzymatic defences against photo-oxidative stress induced by ultraviolet radiation in Arctic marine macroalgae. Polar Biol 25:432–441Google Scholar
  2. Alaiz M, Navarro J, Giron J, Vioque E (1992) Amino acid analysis by high performance liquid chromatography after derivatization with diethylethoxymethylenemalonate. J Chromatogr 591:181–186CrossRefGoogle Scholar
  3. AOAC (2000) Official methods of analysis of AOAC International, 17th ed. Washigton DC, USAGoogle Scholar
  4. Bacchetta C, Rossi A, Ale A, Campana M, Parma M, Cazenave J (2014) Combined toxicological effects of pesticides: a fish multi-biomarker approach. Ecol Indic 36:532–538CrossRefGoogle Scholar
  5. Beutler E (1982) Catalase. In: Beutler E (ed) Red cell metabolism, a manual of biochemical methods. Grune and Stratton Inc., New York, pp 105–106Google Scholar
  6. Bicudo A, Sado R, Cyrino J (2009) Dietary lysine requirement of juvenile pacu Piaractus mesopotamicus (Holmberg, 1887). Aquaculture 297:151–156CrossRefGoogle Scholar
  7. Biller-Takahashi J, Takahashi L, Mingatto F, Urbinati E (2015) The immune system is limited by oxidative stress: dietary selenium promotes optimal antioxidative status and greatest immune defense in pacu Piaractus mesopotamicus. Fish Shellfish Immunol 47:360–367CrossRefGoogle Scholar
  8. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  9. Cabrita M, Vale C, Rauter A (2010) Halogenated compounds from marine algae. Mar Drugs 8:2301–2317CrossRefGoogle Scholar
  10. Cazenave J, Wunderlin D, Hued A, Bistoni M (2005) Haematological parameters in a neotropical fish, Corydoras paleatus (Jenyns, 1842) (Pisces, Callichthyidae) captured from pristine and polluted water. Hydrobiologia 537:25–33CrossRefGoogle Scholar
  11. Chen Y, Sim S, Chiew S, Yeh S, Liou C, Chen J (2012) Dietary administration of a Gracilaria tenuistipitata extract produces protective immunity of white shrimp Litopenaeus vannamei in response to ammonia stress. Aquaculture 370-371:26–31CrossRefGoogle Scholar
  12. Cian R, Martínez-Augustin O, Drago S (2012) Bioactive properties of peptides obtained by enzymatic hydrolysis from protein byproducts of Porphyra columbina. Food Res Int 49:364–372CrossRefGoogle Scholar
  13. Cian R, Alaíz M, Vioque J, Drago S (2013) Enzyme proteolysis enhanced extraction of ACE inhibitory and antioxidant compounds (peptides and polyphenols) from Porphyra columbina residual cake. J Appl Phycol 25:1197–1206CrossRefGoogle Scholar
  14. Cian R, Salgado P, Drago S, González R, Mauri A (2014a) Development of naturally activated edible films with antioxidant properties prepared from red seaweed Porphyra columbina biopolymers. Food Chem 146:6–14CrossRefGoogle Scholar
  15. Cian R, Fajardo M, Alaiz M, Vioque J, González R, Drago S (2014b) Chemical composition, nutritional and antioxidant properties of the red edible seaweed Porphyra columbina. Int J Food Sci Nutr 65:299–305CrossRefGoogle Scholar
  16. Cian R, Garzón A, Betancur Ancona D, Chel Guerrero L, Drago S (2016) Chelating properties of peptides from red seaweed Pyropia columbina and its effect on iron bio-accessibility. Plant Foods Hum Nutr 71:96–101CrossRefGoogle Scholar
  17. Cian R E, Bacchetta C, Cazenave J, Drago SR (2017) Optimization of single screw extrusion process for producing fish feeds based on vegetable meals and evaluation of nutritional effects using a juvenile Piaractus mesopotamicus model. Anim Feed Sci Technol 234:54–64Google Scholar
  18. Cian R, Bacchetta C, Cazenave J, Drago S (2018a) Extruded fish feed with high residual phytase activity and low mineral leaching increased P. mesopotamicus mineral retention. Anim Feed Sci Technol 240:78–87CrossRefGoogle Scholar
  19. Cian R, Llopart E, López-Oliva M, Weisstaub A, Zuleta A, Drago S (2018b) Low level of red seaweed Pyropia columbina added to extruded maize products promotes colonic and systemic antioxidant environment in growing Wistar rats. J Appl Phycol 30:637–648CrossRefGoogle Scholar
  20. CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas) (2005) Marco Ético de Referencia para las Investigaciones Biomédicas en Animales de laboratorio, de granja y obtenidos de la naturaleza, Buenos Aires, Argentina. https://www.web.conicet.gov.ar/documents/11716/0/OCR+RD+20050701-1047.pdf
  21. Duan X, Zhang W, Li X, Wang B (2006) Evaluation of antioxidant property of extract and fractions obtained from a red alga, Polysiphonia urceolata. Food Chem 95:37–43CrossRefGoogle Scholar
  22. Dvir I, Chayoth R, Sod-Moriah U, Shany S, Nyska A, Stark A, Madar Z, Arad S (2000) Soluble polysaccharide and biomass of red microalga Porphyridium sp. alter intestinal morphology and reduce serum cholesterol in rats. Br J Nutr 84:469–476Google Scholar
  23. Estruch R, Sacanella E, Mota F, Chiva-Blanch G, Antúnez E, Casals E, Deulofeu R, Rotilio D, Andres-Lacueva C, Lamuela-Raventos RM, de Gaetano G, Urbano-Marquez A (2011) Moderate consumption of red wine, but not gin, decreases erythrocyte superoxide dismutase activity: a randomised cross-over trial. Nutr Metab Cardiovasc Dis 21:46–53CrossRefGoogle Scholar
  24. Figueiredo F, Encarnação T, Campos M (2016) Algae as functional foods for the elderly. Food Nutr Sci 7:1122–1148Google Scholar
  25. Fleurence J (1999) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Technol 10:25–28CrossRefGoogle Scholar
  26. Goede R, Barton B (1990) Organismic indices and autopsy-based assessment as indicators of health and condition of fish. Am Fish Soc Symp 8:93–108Google Scholar
  27. Gómez-Ordóñez E, Jiménez-Escrig A, Rupérez P (2012) Effect of the red seaweed Mastocarpus stellatus intake on lipid metabolism and antioxidant status in healthy Wistar rats. Food Chem 135:806–811CrossRefGoogle Scholar
  28. Habig W, Pabst M, Jakoby W (1974) Glutathione S transferases. The first step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
  29. Holdt S, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597CrossRefGoogle Scholar
  30. Houston A (1990) Blood and circulation. In: Schreck CB, Moyle PB (eds) Methods for fish biology. American Fisheries Society, Bethesda, pp 273–334Google Scholar
  31. Ighodaro O, Akinloye O (2017) First line defense antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defense grid. Alex J Med.  https://doi.org/10.1016/j.ajme.2017.09.001
  32. Iwai K (2008) Antidiabetic and antioxidant effects of polyphenols in brown alga Ecklonia stolonifera in genetically diabetic KK-Ay mice. Plant Foods Hum Nutr 63:163–169CrossRefGoogle Scholar
  33. Jiménez-Escrig A, Gómez-Ordóñez E, Tenorio M, Rupérez P (2013) Antioxidant and prebiotic effects of dietary fiber co-travelers from sugar Kombu in healthy rats. J Appl Phycol 25:503–512CrossRefGoogle Scholar
  34. Kim K, Bai S, Koo J, Wang X (2002) Effects of dietary Chlorella ellipsoidea supplementation on growth, blood characteristics, and whole-body composition in juvenile Japanese flounder Paralichthys olivaceus. J World Aquacult Soc 33:425–431CrossRefGoogle Scholar
  35. Kim M, Kim J, Choi W, Lee S (2008) Effects of seaweed supplementation on blood glucose concentration, lipid profile, and antioxidant enzyme activities in patients with type 2 diabetes mellitus. Nutr Res Pract 2:62–67CrossRefGoogle Scholar
  36. Kumar S, Brown L (2013) Seaweeds as potential therapeutic interventions for the metabolic syndrome. Rev Endocr Metab Disord 14:299–308CrossRefGoogle Scholar
  37. Kumar C, Ganesan P, Suresh P, Bhaskar N (2008) Seaweeds as a source of nutritionally beneficial compounds-a review. J Food Sci Technol 45:1–13Google Scholar
  38. Leitao C, Marchioni E, Bergaentzlé M, Zhao M, Didierjean L, Taidi B, Ennahar S (2011) Effects of processing steps on the phenolic content and antioxidant activity of beer. J Agric Food Chem 59:1249–1255CrossRefGoogle Scholar
  39. Liu M, Hansen P, Lin X (2011) Bromophenols in marine algae and their bioactivities. Mar Drugs 9:1273–1292CrossRefGoogle Scholar
  40. Llopart E, Cian R, López-Oliva M, Zuleta A, Weisstaub A, Drago S (2017) Colonic and systemic effects of extruded whole-grain sorghum consumption in growing Wistar rats. Br J Nutr 118:589–597CrossRefGoogle Scholar
  41. López-Oliva M, Pozuelo M, Rotger R, Muñoz-Martínez E, Goñi I (2013) Grape antioxidant dietary fibre prevents mitochondrial apoptotic pathways by enhancing Bcl-2 and Bcl-x L expression and minimising oxidative stress in rat distal colonic mucosa. Br J Nutr 109:4–16CrossRefGoogle Scholar
  42. Machado-Neto R, Wiolene M, Mariana C, Jéssica P, Débora B (2018) Growth and hematology of juvenile Piaractus mesopotamicus stocked at 10 up to 40kg/m3 for twenty-one days. Oceanogr Fish Open Access J 8:555733Google Scholar
  43. Machu L, Misurcova L, Ambrozova J, Orsavova J, Mlcek J, Sochor J, Jurikova T (2015) Phenolic content and antioxidant capacity in algal food products. Molecules 20:1118–1133CrossRefGoogle Scholar
  44. Magnoni L, Martos-Sitcha J, Queiroz A, Calduch-Giner J, Gonçalves J, Rocha C, Abreu H, Schrama J, Ozorio R, Pérez-Sánchez J (2017) Dietary supplementation of heat-treated Gracilaria and Ulva seaweeds enhanced acute hypoxia tolerance in gilthead sea bream (Sparus aurata). Biol Open 6:897–908CrossRefGoogle Scholar
  45. Matanjun P, Mohamed S, Muhammad K, Mustapha N (2010) Comparison of cardiovascular protective effects of tropical seaweeds, Kappaphycus alvarezii, Caulerpa lentillifera, and Sargassum polycystum, on high-cholesterol/ high-fat diet in rats. J Med Food 13:792–800CrossRefGoogle Scholar
  46. Misra H, Fridovich (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175Google Scholar
  47. Parma de Croux M (1990) Benzocaine (ethyl-p-aminobenzoate) as an anaesthetic for Prochilodus lineatus, Valenciennes (Pisces, Curimatidae). J Appl Ichthyol 6:189–192CrossRefGoogle Scholar
  48. Peixoto M, Salas-Leitón E, Pereira L, Queiroz A, Magalhães F, Pereira R, Abreu H, Reis P, Gonçalves J, Ozório R (2016) Role of dietary seaweed supplementation on growth performance, digestive capacity and immune and stress responsiveness in European seabass (Dicentrarchus labrax). Aquac Rep 3:189–197CrossRefGoogle Scholar
  49. Qiu Y, Liu Q, Beta T (2010) Antioxidant properties of commercial wild rice and analysis of soluble and insoluble phenolic acids. Food Chem 121:140–147CrossRefGoogle Scholar
  50. Quian Z, Jung W, Kim S (2008) Free radical scavenging activity of a novel antioxidative peptide purified from hydrolysate of bullfrog skin, Rana catesbeiana Shaw. Bioresour Technol 99:1690–1698CrossRefGoogle Scholar
  51. Ragaza J, Koshio S, Mamauag R, Ishikawa M, Yokoyama S, Villamo S (2015) Dietary supplemental effects of red seaweed Eucheuma denticulatum on growth performance, carcass composition and blood chemistry of juvenile Japanese flounder, Paralichthys olivaceus. Aquac Res 46:647–657CrossRefGoogle Scholar
  52. Reichenbach-Klinke H (1980) Enfermedades de los peces. Acribia, ZaragozaGoogle Scholar
  53. Roche H, Bogé G (2000) In vivo effects of phenolic compounds on blood parameters of a marine fish (Dicentrarchus labrax). Comp Biochem Physiol C 125:345–353Google Scholar
  54. Rossi A, Cazenave J, Bacchetta C, Campana M, Parma M (2015) Physiological and metabolic adjustments of Hoplosternum littorale (Teleostei, Callichthyidae) during starvation. Ecol Indic 56:161–170CrossRefGoogle Scholar
  55. Rossi A, Bacchetta C, Cazenave J (2017) Effect of thermal stress on metabolic and oxidative stress biomarkers of Hoplosternum littorale (Teleostei, Callichthyidae). Ecol Indic 79:361–370CrossRefGoogle Scholar
  56. Sabeena Farvin K, Jacobsen C (2013) Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast. Food Chem 138:1670–1681CrossRefGoogle Scholar
  57. Sachindra N, Airanthi M, Hosokawa M, Miyashita K (2010) Radical scavenging and singlet oxygen quenching activity of extracts from Indian seaweeds. J Food Sci Technol 47:94–99CrossRefGoogle Scholar
  58. Sirirustananun N, Chen J, Lin Y, Yeh S, Liou C, Chen L, Sim S, Chiew S (2011) Dietary administration of a Gracilaria tenuistipitata extract enhances the immune response and resistance against Vibrio alginolyticus and white spot syndrome virus in the white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 31:848–855CrossRefGoogle Scholar
  59. Soler-Vila A, Coughlan S, Guiry M (2009) The red alga Porphyra dioica as a fish-feed ingredient for rainbow trout (Oncorhynchus mykiss): effects on growth, feed efficiency, and carcass composition. J Appl Phycol 21:617–624CrossRefGoogle Scholar
  60. Thirunavukkarasu R, Pandiyan P, Balaraman D, Subaramaniyan K, Edward Gnana Jothi G, Manikkam S, Sadaiyappan B (2013) Isolation of bioactive compound from marine seaweeds against fish pathogenic bacteria Vibrio alginolyticus (VA09) and characterisation by FTIR. J Coast Life Med 1:26–33Google Scholar
  61. Tovar J, Bjoerck I, Asp N (1990) Starch content and amylolysis rate in precooked legume flours. J Agric Food Chem 38:1818–1823CrossRefGoogle Scholar
  62. Urbinati E, Goncalves F, Takahashi L (2010) Pacu (Piaractus mesopotamicus). In: Baldisseroto B, Gomes LC (eds) Espécies nativas parapiscicultura no Brasil, second edn. UFSM, Santa Maria, pp 225–246Google Scholar
  63. Valladão G, Gallani S, Pilarski F (2018) South American fish for continental aquaculture. Rev Aquac 10:351–369CrossRefGoogle Scholar
  64. Villanueva M, Morcillo M, Tenorio M, Mateos-Aparicio I, Andrés V, Redondo-Cuenca A (2014) Health-promoting effects in the gut and influence on lipid metabolism of Himanthalia elongata and Gigartina pistillata in hypercholesterolaemic Wistar rats. Eur Food Res Technol 238:409–416CrossRefGoogle Scholar
  65. Whitfield F, Helidoniotis F, Shaw K, Svoronos D (1999) Distribution of bromophenols in species of marine algae from eastern Australia. J Agric Food Chem 47:2367–2373CrossRefGoogle Scholar
  66. 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. Aquac Int 19:1007–1018CrossRefGoogle Scholar
  67. Yagi K (1976) A simple fluorometric assay for lipoperoxide in blood plasma. Biochem Med 15:212–216CrossRefGoogle Scholar
  68. You C, Zhang W, Wang S, Cheng C, Li Y (2014) Evaluation of green alga Ulva pertusa as a dietary ingredient for rabbitfish Siganus canaliculatus juveniles. J Aquac Res 1(1):005Google Scholar
  69. Yuan Y, Walsh N (2006) Antioxidant and antiproliferative activities of extracts from a variety of edible seaweeds. Food Chem Toxicol 44:1144–1150CrossRefGoogle Scholar
  70. Yuan H, Zhang W, Li X, Lü X, Li N, Gao X, Song J (2005) Preparation and in vitro antioxidant activity of κ-carrageenan oligosaccharides and their oversulfated, acetylated, and phosphorylated derivates. Carbohydr Res 340:685–690CrossRefGoogle Scholar
  71. Zdunczyk Z, Frejnagel S, Wróblewska J, Juśkiewicz J, Oszmiański J, Estrella I (2002) Biological activity of polyphenol extracts from different plant sources. Food Res Int 35:183–186CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Instituto de Tecnología de Alimentos, CONICET, FIQ-UNLSanta FeArgentina
  2. 2.Instituto Nacional de Limnología, CONICET-UNLSanta FeArgentina

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