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Fish Physiology and Biochemistry

, Volume 42, Issue 1, pp 203–217 | Cite as

Effects of fish oil replacement by vegetable oil blend on digestive enzymes and tissue histomorphology of European sea bass (Dicentrarchus labrax) juveniles

  • Carolina Castro
  • Ana Couto
  • Amalia Pérez-Jiménez
  • Cláudia R. Serra
  • Patricia Díaz-Rosales
  • Rui Fernandes
  • Geneviève Corraze
  • Stéphane Panserat
  • Aires Oliva-Teles
Article

Abstract

The impact of replacing circa 70 % fish oil (FO) by a vegetable oil (VO) blend (rapeseed, linseed, palm oils; 20:50:30) in diets for European sea bass juveniles (IBW 96 ± 0.8 g) was evaluated in terms of activities of digestive enzymes (amylase, lipase, alkaline phosphatase, trypsin and total alkaline proteases) in the anterior (AI) and posterior (PI) intestine and tissue morphology (pyloric caeca—PC, AI, PI, distal intestine—DI and liver). For that purpose, fish were fed the experimental diets for 36 days and then liver and intestine were sampled at 2, 6 and 24 h after the last meal. Alkaline protease characterization was also done in AI and PI at 6 h post-feeding. Dietary VO promoted higher alkaline phosphatase activity at 2 h post-feeding in the AI and at all sampling points in the PI. Total alkaline protease activity was higher at 6 h post-feeding in the PI of fish fed the FO diet. Identical number of bands was observed in zymograms of alkaline proteases of fish fed both diets. No alterations in the histomorphology of PC, AI, PI or DI were noticed in fish fed the VO diets, while in the liver a tendency towards increased hepatocyte vacuolization due to lipid accumulation was observed. Overall, and with the exception of a higher intestine alkaline phosphatase activity, 70 % FO replacement by a VO blend in diets for European sea bass resulted in no distinctive alterations on the postprandial pattern of digestive enzyme activities and intestine histomorphology.

Keywords

European sea bass Fish Fish oil Postprandial digestive enzyme Tissue histology Vegetable oil 

Notes

Acknowledgments

This work was partially supported by the FCT (Foundation for Science and Technology), Portugal (Project PTDC/MAR-BIO/4107/2012) and co-financed by the European Regional Development Fund (ERDF) through the COMPETE—Operational Competitiveness Programme and national funds through FCT—under the project “PEst-C/MAR/LA0015/2011”. CC was supported by a Grant (SFRH/BD/76297/2011), AC (SFRH/BD/47495/2008) and APJ (SFRH/BPD/64684/2009) from FCT, Portugal. PDR and CRS were supported by Grants (NORTE-07-0124-FEDER-000038-BPD-2013-07; NORTE-07-0124-FEDER-000038-BPD-2013-05, respectively). We express our thanks to Laurence Larroquet for her kind help in the fatty acid analyses of diets and to P. Correia for technical assistance.

References

  1. 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 Physiol Biochem 19:257–267CrossRefGoogle Scholar
  2. Bakke AM, Glover C, Krogdahl Å (2010) Feeding, digestion and absorption of nutrients. In: Grosell M, Farrell AP, Brauner CJ (eds) Fish physiology. Academic Press, London, pp 57–110Google Scholar
  3. Bowyer JN, Qin JG, Adams LR, Thomson MJS, Stone DAJ (2012) The response of digestive enzyme activities and gut histology in yellowtail kingfish (Seriola lalandi) to dietary fish oil substitution at different temperatures. Aquaculture 368–369:19–28CrossRefGoogle Scholar
  4. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye-binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  5. Caballero MJ, Obach A, Rosenlund G, Montero D, Gisvold M, Izquierdo MS (2002) Impact of different lipid sources on growth, lipid digestibility, tissue fatty acid composition and histology of rainbow trout, Oncorhynchus mykiss. Aquaculture 214:253–271CrossRefGoogle Scholar
  6. Caballero MJ, Izquierdo MS, Kjørsvik E, Montero D, Socorro J, Fernández AJ, Rosenlund G (2003) Morphological aspects of intestinal cells from gilthead seabream (Sparus aurata) fed diets containing different lipid sources. Aquaculture 225:325–340CrossRefGoogle Scholar
  7. Caballero MJ, Izquierdo MS, Kjørsvik E, Fernández E, Rosenlund G (2004) Histological alterations in the liver of sea bream, Sparus aurata L., caused by short- or long-term feeding with vegetable oils. Recovery of normal morphology after feeding fish oil as the sole lipid source. J Fish Dis 27:531–541CrossRefPubMedGoogle Scholar
  8. Caballero MJ, Gallardo G, Robaina L, Montero D, Fernández A, Izquierdo MS (2006) Vegetable lipid sources affect in vitro biosynthesis of triacylglycerols and phospholipids in the intestine of seabream (Sparus aurata). Br J Nutr 95:448–454CrossRefPubMedGoogle Scholar
  9. Cahu CL, Infante JLZ, Corraze G, Coves D (2000) Dietary lipid level affects fatty acid composition and hydrolase activities of intestinal brush border membrane in sea bass. Fish Physiol Biochem 23:165–172CrossRefGoogle Scholar
  10. Caruso G, Denaro MG, Genovese L (2008) Temporal changes in digestive enzyme activities in the gastrointestinal tract of European eel (Anguilla anguilla) (Linneo 1758) following feeding. Mar Freshw Behav Phys 41:215–228CrossRefGoogle Scholar
  11. Castro C, Pérez-Jiménez A, Coutinho F, Pousão-Ferreira P, Brandão TM, Oliva-Teles A, Peres H (2013) Digestive enzymes of meagre (Argyrosomus regius) and white seabream (Diplodus sargus). Effects of dietary brewer’s spent yeast supplementation. Aquaculture 416–417:322–327CrossRefGoogle Scholar
  12. Castro C, Corraze G, Panserat S, Oliva-Teles A (2015a) Effects of fish oil replacement by a vegetable oil blend on digestibility, postprandial serum metabolite profile, lipid and glucose metabolism of European sea bass (Dicentrarchus labrax) juveniles. Nutr, Aquac. doi: 10.1111/anu.12184 Google Scholar
  13. Castro C, Corraze G, Pérez-Jiménez A, Larroquet L, Cluzeaud M, Panserat S, Oliva-Teles A (2015b) Dietary carbohydrate and lipid source affect cholesterol metabolism of European sea bass (Dicentrarchus labrax) juveniles. Br J Nutr 1–14. doi: 10.1017/S0007114515002731
  14. Chikwati EM, Sahlmann C, Holm H, Penn MH, Krogdahl Å, Bakke AM (2013) Alterations in digestive enzyme activities during the development of diet-induced enteritis in Atlantic salmon Salmo salar L. Aquaculture 402–403:28–37CrossRefGoogle Scholar
  15. Ducasse-Cabanot S, Zambonino-Infante J, Richard N, Médale F, Corraze G, Mambrini M, Robin J, Cahu C, Kaushik S, Panserat S (2007) Reduced lipid intake leads to changes in lipid digestive enzymes in the intestine but has minor effects on key enzymes of hepatic intermediary metabolism in rainbow trout (Oncorhynchus mykiss). Animal 1:1272–1282CrossRefPubMedGoogle Scholar
  16. Einarsson S, Davies PS, Talbot C (1996) The effect of feeding on the secretion of pepsin, trypsin and chymotrypsin in the Atlantic salmon, Salmo salar L. Fish Physiol Biochem 15:439–446CrossRefPubMedGoogle Scholar
  17. Faulk CK, Benninghoff AD, Holt GJ (2007) Ontogeny of the gastrointestinal tract and selected digestive enzymes in cobia Rachycentron canadum (L.). J Fish Biol 70:567–583CrossRefGoogle Scholar
  18. Fernández I, Moyano FJ, Díaz M, Martínez TF (2001) Characterization of α-amylase activity in five species of Mediterranean sparid fishes (Sparidae, Teleostei). J Exp Mar Biol Ecol 262:1–12CrossRefGoogle Scholar
  19. Figueiredo-Silva A, Rocha E, Dias J, Silva P, Rema P, Gomes E, Valente LMP (2005) Partial replacement of fish oil by soybean oil on lipid distribution and liver histology in European sea bass (Dicentrarchus labrax) and rainbow trout (Oncorhynchus mykiss) juveniles. Aquac Nutr 11:147–155CrossRefGoogle Scholar
  20. Fountoulaki E, Alexis MN, Nengas I, Venou B (2005) Effect of diet composition on nutrient digestibility and digestive enzyme levels of gilthead sea bream (Sparus aurata L.). Aquac Res 36:1243–1251CrossRefGoogle Scholar
  21. Fountoulaki E, Vasilaki A, Hurtado R, Grigorakis K, Karacostas I, Nengas I, Rigos G, Kotzamanis Y, Venou B, Alexis MN (2009) Fish oil substitution by vegetable oils in commercial diets for gilthead sea bream (Sparus aurata L.); effects on growth performance, flesh quality and fillet fatty acid profile: recovery of fatty acid profiles by a fish oil finishing diet under fluctuating water temperatures. Aquaculture 289:317–326CrossRefGoogle Scholar
  22. Furné M, Hidalgo MC, López A, García-Gallego M, Morales AE, Domenzain A, Domezain J, Sanz A (2005) Digestive enzyme activities in Adriatic sturgeon Acipenser naccarii and rainbow trout Oncorhynchus mykiss. A comparative study. Aquaculture 250:391–398CrossRefGoogle Scholar
  23. García-Carreño FL, Dimes LE, Haard NF (1993) Substrate gel-electrophoresis for composition and molecular-weight of proteinases of proteinaceous proteinase-inhibitors. Anal Biochem 214:65–69CrossRefPubMedGoogle Scholar
  24. Geurden I, Jutfelt F, Olsen R, Sundell K (2009) A vegetable oil feeding history affects digestibility and intestinal fatty acid uptake in juvenile rainbow trout Oncorhynchus mykiss. Comp Biochem Physiol A 152:552–559CrossRefGoogle Scholar
  25. Hartviksen M, Bakke AM, Vecino JG, Ringo E, Krogdahl A (2014) Evaluation of the effect of commercially available plant and animal protein sources in diets for Atlantic salmon (Salmo salar L.): digestive and metabolic investigations. Fish Physiol Biochem 40:1621–1637CrossRefPubMedGoogle Scholar
  26. Hidalgo MC, Urea E, Sanz A (1999) Comparative study of digestive enzymes in fish with different nutritional habits. Proteolytic and amylase activities. Aquaculture 170:267–283CrossRefGoogle Scholar
  27. Jordal AEO, Lie O, Torstensen BE (2007) Complete replacement of dietary fish oil with a vegetable oil blend effects liver and plasma lipoprotein levels in Atlantic salmon (Salmo salar). Aquac Nutr 13:114–130CrossRefGoogle Scholar
  28. Jutfelt F, Olsen RE, Björnsson BTh, Sundell K (2007) Parr–smolt transformation and dietary vegetable lipids affect intestinal nutrient uptake, barrier function and plasma cortisol levels in Atlantic salmon. Aquaculture 273:298–311CrossRefGoogle Scholar
  29. Kjaer MA, Vegusdal A, Gjøen T, Rustan AC, Todorčević M, Ruyter B (2008) Effect of rapeseed oil and dietary n-3 fatty acids on triacylglycerol synthesis and secretion in Atlantic salmon hepatocytes. Biochim Biophys Acta 1781:112–122CrossRefPubMedGoogle Scholar
  30. Koven WM, Henderson RJ, Sargent JR (1994) Lipid digestion in turbot (Scophtalmus maximus): I. Lipid class and fatty acid composition of digesta from different segments of the digestive tract. Fish Physiol Biochem 13:69–79CrossRefPubMedGoogle Scholar
  31. Kowalska A, Zakés Z, Jankowska B, Siwicki A (2010) Impact of diets with vegetable oils on the growth, histological structure of internal organs, biochemical blood parameters, and proximate composition of pikeperch Sander lucioperca (L.). Aquaculture 301:69–77CrossRefGoogle Scholar
  32. Krogdahl Å, Bakke-McKellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquac Nutr 9:361–371CrossRefGoogle Scholar
  33. Krogdahl Å, Hemre GI, Mommsen TP (2005) Carbohydrates in fish nutrition: digestion and absorption in postlarval stages. Aquac Nutr 11:103–122CrossRefGoogle Scholar
  34. Kuz’mina VV (2008) Classical and modern concepts in fish digestion. In: Cyrino JEP, Bureau DP, Kapoor BG (eds) Feeding and digestive functions of fishes. Science Publishers, Enfield, pp 85–154CrossRefGoogle Scholar
  35. Laemmli UK (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227:680–688CrossRefPubMedGoogle Scholar
  36. Leaver MJ, Villeneuve LAN, Obach A, Jensen L, Bron JE, Tocher DR, Taggart JB (2008) Functional genomics reveals increases in cholesterol biosynthetic genes and highly unsaturated fatty acid biosynthesis after dietary substitution of fish oil with vegetable oils in Atlantic salmon (Salmo salar). BMC Genom 9:299CrossRefGoogle Scholar
  37. Menoyo D, Izquierdo MS, Robaina L, Ginés R, Lopez-Bote CJ, Bautista JM (2004) Adaptation of lipid metabolism, tissue composition, and flesh quality in gilthead sea bream (Sparus aurata) to the replacement of dietary fish oil by linseed and soybean oils. Br J Nutr 92:41–52CrossRefPubMedGoogle Scholar
  38. Moldal T, Løkka G, Wiik-Nielsen J, Austbø L, Torstensen BE, Rosenlund G, Dale OB, Kaldhusdal M, Koppang EO (2014) Substitution of dietary fish oil with plant oils is associated with shortened mid intestinal folds in Atlantic salmon (Salmo salar). BMC Vet Res 10:60PubMedCentralCrossRefPubMedGoogle Scholar
  39. Morais S, Cahu C, Zambonino-Infante J, Robin J, Rønnestad I, Dinis M, Conceição L (2004) Dietary TAG source and level affect performance and lipase expression in larval sea bass (Dicentrarchus labrax). Lipids 39:449–458CrossRefPubMedGoogle Scholar
  40. Morais S, Caballero MJ, Conceição LEC, Izquierdo MS, Dinis MT (2006) Dietary neutral lipid level and source in Senegalese sole (Solea senegalensis) larvae: effect on growth, lipid metabolism and digestive capacity. Comp Biochem Physiol B 144:57–69CrossRefPubMedGoogle Scholar
  41. Morais S, Pratoomyot J, Taggart JB, Bron JE, Guy DR, Bell JG, Tocher DR (2011) Genotype-specific responses in Atlantic salmon (Salmo salar) subject to dietary fish oil replacement by vegetable oil: a liver transcriptomic analysis. BMC Genom 12:255CrossRefGoogle Scholar
  42. Mourente G, Good JE, Bell JG (2005) Partial substitution of fish oil with rapeseed, linseed and olive oils in diet for European sea bass (Dicentrarchus labrax L.) effects on flesh fatty acid composition, plasma prostaglandins E2 and F2a, immune function and effectiveness of a fish oil finishing diet. Aquac Nutr 11:25–40CrossRefGoogle Scholar
  43. Mourente G, Good JE, Thompson KD, Bell JG (2007) Effects of partial substitution of dietary fish oil with blends of vegetable oils, on blood leucocyte fatty acid compositions, immune function and histology in European sea bass (Dicentrarchus labrax L.). Br J Nutr 98:770–779CrossRefPubMedGoogle Scholar
  44. Moyano FJ, Díaz M, Alarcón FJ, Sarasquete MC (1996) Characterization of digestive enzyme activity during larval development of gilthead seabream (Sparus aurata). Fish Physiol Biochem 15:121–130CrossRefPubMedGoogle Scholar
  45. Munilla-Morán R, Saborido-Rey F (1996a) Digestive enzymes in marine species. I. Proteinase activities in gut from redfish (Sebastes mentella), seabream (Sparus aurata) and turbot (Scophthalmus maximus). Comp Biochem Physiol B 113:395–402CrossRefGoogle Scholar
  46. Munilla-Morán R, Saborido-Rey F (1996b) Digestive enzymes in marine species. II. Amylase activities in gut from seabream (Sparus aurata), turbot (Scophthalmus maximus) and redfish (Sebastes mentella). Comp Biochem Physiol B 113:827–834CrossRefGoogle Scholar
  47. Nordrum S, Krogdahl Å, Røsjø C, Olli JJ, Holm H (2000) Effects of methionine, cysteine and medium chain triglycerides on nutrient digestibility, absorption of amino acids along the intestinal tract and nutrient retention in Atlantic salmon (Salmo salar L.) under pair-feeding regime. Aquaculture 186:341–360CrossRefGoogle Scholar
  48. Olsen RE, Ringø E (1997) Lipid digestibility in fish: a review. Recent Res Dev Lipid Res 1:199–265Google Scholar
  49. Olsen RE, Myklebust R, Kaino T, Ringo E (1999) Lipid digestibility and ultrastructural changes in the enterocytes of Arctic charr (Salvelinus alpinus L.) fed linseed oil and soybean lecithin. Fish Physiol Biochem 21:35–44CrossRefGoogle Scholar
  50. Olsen RE, Dragnes BT, Myklebust R, Ringø E (2003) Effect of soybean oil and soybean lecithin on intestinal lipid composition and lipid droplet accumulation of rainbow trout, Oncorhynchus mykiss Walbaum. Fish Physiol Biochem 29:327–329CrossRefGoogle Scholar
  51. Peng M, Xu W, Mai K, Zhou H, Zhang Y, Liufu Z, Zhang K, Ai Q (2014) Growth performance, lipid deposition and hepatic lipid metabolism related gene expression in juvenile turbot (Scophthalmus maximus L.) fed diets with various fish oil substitution levels by soybean oil. Aquaculture 433:442–449CrossRefGoogle Scholar
  52. Pérez-Jiménez A, Cardenete G, Morales AE, García-Alcázar A, Abellán E, Hidalgo MC (2009) Digestive enzymatic profile of Dentex dentex and response to different dietary formulations. Comp Biochem Physiol A 154:157–164CrossRefGoogle Scholar
  53. Regost C, Arzel J, Robin J, Rosenlund G, Kaushik SJ (2003) Total replacement of fish oil by soybean or linseed oil with a return to fish oil in turbot (Psetta maxima). I. Growth performance, flesh fatty acid profile, and lipid metabolism. Aquaculture 217:465–482CrossRefGoogle Scholar
  54. Ribeiro L, Moura J, Santos M, Colen R, Rodrigues V, Bandarra N, Soares F, Ramalho P, BarataM Moura P, Pousão-Ferreira P, Dias J (2015) Effect of vegetable based diets on growth, intestinal morphology, activity of intestinal enzymes and haematological stress indicators in meagre (Argyrosomus regius). Aquaculture. doi: 10.1016/j.aquaculture.2014.12.017 Google Scholar
  55. Richard N, Kaushik S, Larroquet L, Panserat S, Corraze G (2006a) Replacing dietary fish oil by vegetable oils has little effects on lipogenesis, lipid transport and tissue lipid uptake in rainbow trout (Oncorhynchus mykiss). Br J Nutr 96:299–309CrossRefPubMedGoogle Scholar
  56. Richard N, Mourente G, Kaushik S, Corraze G (2006b) Replacement of a large portion of fish oil by vegetable oils does not affect lipogenesis, lipid transport and tissue lipid uptake in European seabass (Dicentrachus labrax L.). Aquaculture 261:1077–1087CrossRefGoogle Scholar
  57. Rodiles A, Santigosa E, Herrera M, Hachero-Cruzado I, Cordero ML, Martínez-Llorens S, Lall SP, Alarcón FJ (2012) Effect of dietary protein level and source on digestive proteolytic enzyme activity in juvenile Senegalese sole, Solea senegalensis Kaup 1850. Aquacult Int 20:1053–1070CrossRefGoogle Scholar
  58. Ruyter B, Moya-Falcón C, Rosemlund G, Vegusdal A (2006) Fat content and morphology of liver and intestine of Atlantic salmon (Salmo salar): effects of temperature and soybean oil. Aquaculture 252:441–452CrossRefGoogle Scholar
  59. Santigosa E, Sánchez J, Médale F, Kaushik S, Pérez-Sánchez J, Gallardo MA (2008) Modifications of digestive enzymes in trout (Oncorhynchus mykiss) and seabream (Sparus aurata) in response to dietary fish meal replacement by plant protein sources. Aquaculture 282:68–74CrossRefGoogle Scholar
  60. Santigosa E, García-Meilán I, Valentín JM, Navarro I, Pérez-Sánchez J, Gallardo MÁ (2011) Plant oils’ inclusion in high fish meal-substituted diets: effect on digestion and nutrient absorption in gilthead sea bream (Sparus aurata L.). Aquac Res 42:962–974CrossRefGoogle Scholar
  61. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184CrossRefGoogle Scholar
  62. Torstensen BE, Froyland L, Lie O (2004) Replacing dietary fish oil with increasing levels of rapeseed oil and olive oil-effects on Atlantic salmon (Salmo salar L.) tissue and lipoprotein lipid composition and lipogenic enzyme activities. Aquac Nutr 10:175–192CrossRefGoogle Scholar
  63. Walter HE (1984) Proteinases: methods with hemoglobin, casein and azocoll as substrates. In: Bergmeyer HJ (ed) Methods of enzymatic analysis, vol V. Verlag Chemie, Weinham, pp 270–277Google Scholar
  64. Wassef EA, Wahby OM, Sakr EM (2007) Effect of dietary vegetable oils on health and liver histology of gilthead seabream (Sparus aurata) growers. Aquac Res 38:852–861CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Carolina Castro
    • 1
    • 2
  • Ana Couto
    • 1
    • 2
  • Amalia Pérez-Jiménez
    • 1
  • Cláudia R. Serra
    • 1
  • Patricia Díaz-Rosales
    • 1
  • Rui Fernandes
    • 3
  • Geneviève Corraze
    • 4
  • Stéphane Panserat
    • 4
  • Aires Oliva-Teles
    • 1
    • 2
  1. 1.CIMAR/CIIMAR- Centro Interdisciplinar de Investigação Marinha e AmbientalUniversidade do PortoPortoPortugal
  2. 2.Departamento de Biologia, Faculdade de CiênciasUniversidade do PortoPortoPortugal
  3. 3.IBMC - Instituto de Biologia Molecular e CelularUniversidade do PortoPortoPortugal
  4. 4.INRA, UR1067 Nutrition Metabolism AquacultureSaint-Pée-sur-NivelleFrance

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