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Dietary lipid concentrations influence growth, body composition, morphology of the liver and mid-intestine, and antioxidant status of marbled eel (Anguilla marmorata)

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Abstract

An 8-week feeding trial was conducted to explore the effect of dietary lipid concentrations on growth, body composition, morphology of liver, and mid-intestine and antioxidant status in marbled eel (Anguilla marmorata). Fish (initial average weight 6.86 ± 0.11 g) were held in 18 tanks (inside diameter 80 cm, height 60 cm, volume 300 L, 25 fish/tank), with triplicate treatment groups being fed to apparent satiation twice each day on isonitrogenous (421 g/kg crude protein) diets containing different concentrations of lipid (41.2, 73.9, 113.9, 146.2, 178.1, and 216.7 g/kg). The sampling procedure was implemented after 24 h of fasting. Fish fed the diets with 178.1 and 216.7 g lipid/kg grew better than fish fed the other diets. The lowest feed intake and the highest feed conversion rate were found in 41.2 g/kg group. Muscle lipid concentrations and heights of intestinal folds, enterocytes, and microvilli in mid-intestine increased as dietary lipid concentrations increased from 41.2 to 178.1 g/kg. Hepatocyte hypertrophy and lipid vacuolization were seen in liver of the fish fed 216.7 g/kg diet. Based on broken-line analysis of serum total antioxidant capacity and quadratic regression analysis of serum glutathione peroxidase and catalase, it was concluded that dietary lipid concentrations of 125.5–159.2 g/kg promoted antioxidant status. A broken-line analysis of data for specific growth rate and weight gain gave an estimated optimal dietary lipid concentration of 195.3–198.7 g/kg. Marbled eel had quite a high demand for dietary lipid to support good growth, but excessive lipid level (216.7 g/kg) may have an adverse impact on liver structure. Moreover, marbled eel may not tolerate high concentration of dietary carbohydrate.

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All the data in the article are available from the corresponding author upon reasonable request.

References

  • Alpsoy L, Yildirim A, Agar G (2009) The antioxidant effects of vitamin A, C, and E on aflatoxin B1-induced oxidative stress in human lymphocytes. Toxicol Ind Health 25:121–127

    CAS  PubMed  Google Scholar 

  • Association of Official Analytical Chemists (AOAC) (1997) Official Methods of Analysis of Official Analytical Chemists International, sixteenth edn. Association of Official Analytical Chemists, Arlington

    Google Scholar 

  • Atencio L, Moreno I, Jos A, Prieto AI, Moyano R, Blanco A, Camean AM (2009) Effects of dietary selenium on the oxidative stress and pathological changes in tilapia (Oreochromis niloticus) exposed to a microcystin-producing cyanobacterial water bloom. Toxicon 53:269–282

    CAS  PubMed  Google Scholar 

  • Aursand M, Bleivik B, Rainuzzo JR, Jørgensen L, Mohr V (1994) Lipid distribution and composition of commercially farmed Atlantic salmon (Salmo salar). J Sci Food Agric 64:239–248

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Caspary WF (1992) Physiology and pathophysiology of intestinal absorption. Am J Clin Nutr 55:299S–308S

    CAS  PubMed  Google Scholar 

  • Chatzifotis S, Panagiotidou M, Papaioannou N, Pavlidis M, Nengas I, Mylonas CC (2010) Effect of dietary lipid levels on growth, feed utilization, body composition and serum metabolites of meagre (Argyrosomus regius) juveniles. Aquaculture 307:65–70

    CAS  Google Scholar 

  • Cheng Z, Buentello A, Gatlin DM III (2011) Dietary nucleotides influence immune responses and intestinal morphology of red drum Sciaenops ocellatus. Fish Shellfish Immun 30:143–147

    CAS  Google Scholar 

  • Chou BS, Shiau SY (1996) Optimal dietary lipid level for growth of juvenile hybrid tilapia, Oreochromis niloticus × Oreochromis aureus. Aquaculture 143:185–195

    CAS  Google Scholar 

  • Chou RL, Su MS, Chen HY (2001) Optimal dietary protein and lipid levels for juvenile cobia (Rachycentron canadum). Aquaculture 193:81–89

    CAS  Google Scholar 

  • De Silva SS, Gunasekera RM, Gooley G, Ingram BA (2001) Growth of Australian shortfin eel (Anguilla australis) elvers given different dietary protein and lipid levels. Aquac Nutr 7:53–57

    Google Scholar 

  • Du ZY et al (2008) Utilization of different dietary lipid sources at high level in herbivorous grass carp (Ctenopharyngodon idella): mechanism related to hepatic fatty acid oxidation. Aquac Nutr 14:77–92

    CAS  Google Scholar 

  • Du ZY, Liu YJ, Tian LX, Wang JT, Wang Y, Liang GY (2005) Effect of dietary lipid level on growth, feed utilization and body composition by juvenile grass carp (Ctenopharyngodon idella). Aquac Nutr 11:139–146

    CAS  Google Scholar 

  • Engin K, Carter C (2001) Ammonia and urea excretion rates of juvenile Australian short-finned eel (Anguilla australis australis) as influenced by dietary protein level. Aquaculture 194:123–136

    CAS  Google Scholar 

  • Fan HP (2009) A survey on the introduction and rearing test of new culture eel species in China. Sci Fish Farming 12:2–3 (in Chinese)

    Google Scholar 

  • Food and Agriculture Organization of the United Nations (FAO) (2016) Global aquaculture production statistics in 2016. In: Cultured Aquatic Species Information Programme. Fisheries and Aquaculture Department, Rome.

  • Franzén LE, Ekstedt M, Kechagias S, Bodin L (2005) Semiquantitative evaluation overestimates the degree of steatosis in liver biopsies: a comparison to stereological point counting. Mod Pathol 18:912–916

    PubMed  Google Scholar 

  • Gaetani GF, Ferraris A, Rolfo M, Mangerini R, Arena S, Kirkman H (1996) Predominant role of catalase in the disposal of hydrogen peroxide within human erythrocytes. Blood 87:1595–1599

    CAS  PubMed  Google Scholar 

  • Gallego MG, Hidalgo MC, Suarez MD, Sanz A, De La Higuera M (1993) Feeding of the european eel Anguilla anguilla II. Influence of dietary lipid level. Comp Biochem Phys A 105:171–175

    Google Scholar 

  • Gao YJ, Yang HJ, Liu YJ, Chen SJ, Guo DQ, Yu YY, Tian LX (2014) Effects of graded levels of threonine on growth performance, biochemical parameters and intestine morphology of juvenile grass carp Ctenopharyngodon idella. Aquaculture 424-425:113–119

    CAS  Google Scholar 

  • Gélineau A, Corraze G, Boujard T, Larroquet L, Kaushik S (2001) Relation between dietary lipid level and voluntary feed intake, growth, nutrient gain, lipid deposition and hepatic lipogenesis in rainbow trout. Reprod Nutr Dev 41:487–504

    PubMed  Google Scholar 

  • Guo JL, Zhou YL, Zhao H, Chen WY, Chen YJ, Lin SM (2019) Effect of dietary lipid level on growth, lipid metabolism and oxidative status of largemouth bass, Micropterus salmoides. Aquaculture 506:394–400

    CAS  Google Scholar 

  • Hansen J et al (2008) Apparent digestion and apparent retention of lipid and fatty acids in Atlantic cod (Gadus morhua) fed increasing dietary lipid levels. Aquaculture 284:159–166

    CAS  Google Scholar 

  • Higgs D, Dong F (2000) Lipids and fatty acids. In: Stickney RR (ed) book: Encyclopedia of Aquaculture. Wiley, New York, pp 476–496

    Google Scholar 

  • Hillestad M, Johnsen F (1994) High-energy/low-protein diets for Atlantic salmon: effects on growth, nutrient retention and slaughter quality. Aquaculture 124:109–116

    Google Scholar 

  • Jin Y, Tian LX, Zeng SL, Xie SW, Yang HJ, Liang GY, Liu YJ (2013) Dietary lipid requirement on non-specific immune responses in juvenile grass carp (Ctenopharyngodon idella). Fish Shellfish Immun 34:1202–1208

    CAS  Google Scholar 

  • Kikuchi K, Furuta T, Iwata N, Onuki K, Noguchi T (2009) Effect of dietary lipid levels on the growth, feed utilization, body composition and blood characteristics of tiger puffer Takifugu rubripes. Aquaculture 298:111–117

    CAS  Google Scholar 

  • Lee SM, Jeon IG, Lee JY (2002) Effects of digestible protein and lipid levels in practical diets on growth, protein utilization and body composition of juvenile rockfish (Sebastes schlegeli). Aquaculture 211:227–239

    CAS  Google Scholar 

  • Lee SM, Kim KD (2005) Effect of various levels of lipid exchanged with dextrin at different protein level in diet on growth and body composition of juvenile flounder Paralichthys olivaceus. Aquac Nutr 11:435–442

    CAS  Google Scholar 

  • Lewis-McCrea LM, Lall SP (2007) Effects of moderately oxidized dietary lipid and the role of vitamin E on the development of skeletal abnormalities in juvenile Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 262:142–155

    CAS  Google Scholar 

  • Liang F, Zhang G, Yin S, Wang L (2016) The role of three heat shock protein genes in the immune response to Aeromonas hydrophila challenge in marbled eel, Anguilla marmorata. R Soc Open Sci 3:160375

    PubMed  PubMed Central  Google Scholar 

  • Lin YH, Shiau SY (2003) Dietary lipid requirement of grouper, Epinephelus malabaricus, and effects on immune responses. Aquaculture 225:243–250

    CAS  Google Scholar 

  • Lu KL, Xu WN, Li XF, Liu WB, Wang LN, Zhang CN (2013) Hepatic triacylglycerol secretion, lipid transport and tissue lipid uptake in blunt snout bream (Megalobrama amblycephala) fed high-fat diet. Aquaculture 408-409:160–168

    CAS  Google Scholar 

  • Luo M, Guan R, Li Z, Jin H (2013) The effects of water temperature on the survival, feeding, and growth of the juveniles of Anguilla marmorata and A. bicolor pacifica. Aquaculture 400:61–64

    Google Scholar 

  • Luo Z, Liu YJ, Mai KS, Tian LX, Liu DH, Tan XY, Lin HZ (2005) Effect of dietary lipid level on growth performance, feed utilization and body composition of grouper Epinephelus coioides juveniles fed isonitrogenous diets in floating netcages. Aquac Int 13:257–269

    CAS  Google Scholar 

  • Lushchak VI (2011) Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp Biochem Physiol C 153:175–190

    Google Scholar 

  • Mamauag REP, Ragaza JA, Nacionales TJ (2017) Nutritional evaluation of distiller’s dried grain with soluble as replacement to soybean meal in diets of milkfish, Chanos chanos and its effect on fish performance and intestinal morphology. Aquac Nutr 23:1027–1034

    CAS  Google Scholar 

  • Manjappa K, Keshavanath P, Gangadhara B (2002) Growth performance of common carp, Cyprinus carpio fed varying lipid levels through low protein diet, with a note on carcass composition and digestive enzyme activity. Acta Ichthyol Piscat 32:145–155

    Google Scholar 

  • Martins DA, Valente LMP, Lall SP (2007) Effects of dietary lipid level on growth and lipid utilization by juvenile Atlantic halibut (Hippoglossus hippoglossus, L.). Aquaculture 263:150–158

    CAS  Google Scholar 

  • Meng Y, Ma R, Ma J, Han D, Xu W, Zhang W, Mai K (2017) Dietary nucleotides improve the growth performance, antioxidative capacity and intestinal morphology of turbot (Scophthalmus maximus). Aquac Nutr 23:585–593

    CAS  Google Scholar 

  • Meng YQ, Qian K, Ma R, Liu X, Han B, Wu J, Zhang L, Zhan T, Hu X, Tian H, Li C (2019) Effects of dietary lipid levels on sub-adult triploid rainbow trout (Oncorhynchus mykiss): growth performance, digestive ability, health status and expression of growth-related genes. Aquaculture 513:734394

    CAS  Google Scholar 

  • Nanton DA, Lall SP, McNiven MA (2001) Effects of dietary lipid level on liver and muscle lipid deposition in juvenile haddock, Melanogrammus aeglefinus L. Aquac Res 32:225–234

    CAS  Google Scholar 

  • Nayak M, Saha A, Pradhan A, Samanta M, Mohanty TK, Giri SS (2018) Influence of dietary lipid levels on growth, nutrient utilization, tissue fatty acid composition and desaturase gene expression in silver barb (Puntius gonionotous) fingerlings. Comp Biochem Phys Part B 226:18–25

    CAS  Google Scholar 

  • NRC (2011) Lipids. In: Nutrient requirements of fish and shrimp. The National Academies Press, Washington DC, pp 102–134

    Google Scholar 

  • Okamura A, Yamada Y, Horie N, Utoh T, Mikawa N, Tanaka S, Tsukamoto K (2007) Effects of water temperature on early development of Japanese eel Anguilla japonica. Fish Sci 73:1241–1248

    CAS  Google Scholar 

  • Pan CH, Chien YH, Hunter B (2003) The resistance to ammonia stress of Penaeus monodon Fabricius juvenile fed diets supplemented with astaxanthin. J Exp Mar Biol Ecol 297:107–118

    CAS  Google Scholar 

  • Peres H, Oliva-Teles A (1999) Effect of dietary lipid level on growth performance and feed utilization by European sea bass juveniles (Dicentrarchus labrax). Aquaculture 179:325–334

    CAS  Google Scholar 

  • Qiang J, He J, Yang H, Sun Y, Tao Y, Xu P, Zhu Z (2017) Dietary lipid requirements of larval genetically improved farmed tilapia, Oreochromis niloticus (L.), and effects on growth performance, expression of digestive enzyme genes, and immune response. Aquac Res 48:2827–2840

    CAS  Google Scholar 

  • Rašković BS, Stanković MB, Marković ZZ, Poleksić VD (2011) Histological methods in the assessment of different feed effects on liver and intestine of fish. J Agric Sci 56:87–100

    Google Scholar 

  • Regost C, Arzel J, Cardinal M, Robin J, Laroche M, Kaushik SJ (2001) Dietary lipid level, hepatic lipogenesis and flesh quality in turbot (Psetta maxima). Aquaculture 193:291–309

    CAS  Google Scholar 

  • Rueda-López S, Lazo JP, Reyes GC, Viana MT (2011) Effect of dietary protein and energy levels on growth, survival and body composition of juvenile Totoaba macdonaldi. Aquaculture 319:385–390

    Google Scholar 

  • Sato N, Nakano T, Kawakami H, Idota T (1999) In vitro and in vivo effects of exogenous nucleotides on the proliferation and maturation of intestinal epithelial cells. J Nutr Sci Vitaminol 45:107–118

    CAS  PubMed  Google Scholar 

  • Shiau SY, Su SL (2005) Juvenile tilapia (Oreochromis niloticus × Oreochromis aureus) requires dietary myo-inositol for maximal growth. Aquaculture 243:273–277

    CAS  Google Scholar 

  • Song LP, An L, Zhu YA, Li X, Wang AY (2009) Effects of dietary lipids on growth and feed utilization of jade perch, Scortum barcoo. J World Aquacult Soc 40:266–273

    Google Scholar 

  • Tibbetts SM, Lall SP, Anderson DM (2000) Dietary protein requirement of juvenile American eel (Anguilla rostrata) fed practical diets. Aquaculture 186:145–155

    CAS  Google Scholar 

  • Torstensen B, Lie Ø, Hamre K (2001) A factorial experimental design for investigation of effects of dietary lipid content and pro- and antioxidants on lipid composition in Atlantic salmon (Salmo salar) tissues and lipoproteins. Aquac Nutr 7:265–276

    CAS  Google Scholar 

  • Vergara J, Lopez-Calero G, Robaina L, Caballero M, Montero D, Izquierdo M, Aksnes A (1999) Growth, feed utilization and body lipid content of gilthead seabream (Sparus aurata) fed increasing lipid levels and fish meals of different quality. Aquaculture 179:35–44

    CAS  Google Scholar 

  • Wang JT, Liu YJ, Tian LX, Mai KS, Du ZY, Wang Y, Yang HJ (2005) Effect of dietary lipid level on growth performance, lipid deposition, hepatic lipogenesis in juvenile cobia (Rachycentron canadum). Aquaculture 249:439–447

    CAS  Google Scholar 

  • Wang LN, Liu WB, Lu KL, Xu WN, Cai DS, Zhang CN, Qian Y (2014) Effects of dietary carbohydrate/lipid ratios on non-specific immune responses, oxidative status and liver histology of juvenile yellow catfish Pelteobagrus fulvidraco. Aquaculture 426:41–48

    Google Scholar 

  • Xu WN, Li JY, Li XF, Huang GQ, Liu WB (2013) Alterations of liver histology and blood biochemistry in blunt snout bream Megalobrama amblycephala fed high-fat diets. Fish Sci 79:661–671

    Google Scholar 

  • Yan J, Liao K, Wang TJ, Mai KS, Xu W, Ai QH (2015) Dietary lipid levels influence lipid deposition in the liver of large yellow croaker (Larimichthys crocea) by regulating lipoprotein receptors, fatty acid uptake and triacylglycerol synthesis and catabolism at the transcriptional level. PLoS One 10:e0129937

    PubMed  PubMed Central  Google Scholar 

  • Yigit M, Yardim Ö, Koshio S (2002) The protein sparing effects of high lipid levels in diets for rainbow trout (Oncorhynchus mykiss, W. 1792) with special reference to reduction of total nitrogen excretion. Isr J Aquacult-Bamid 54:79–88

    Google Scholar 

  • Yoshii K, Takakuwa F, Nguyen HP, Masumoto T, Fukada H (2010) Effect of dietary lipid level on growth performance and feed utilization of juvenile kelp grouper Epinephelus bruneus. Fish Sci 76:139–145

    CAS  Google Scholar 

  • Zheng JL, Luo Z, Zhu QL, Tan XY, Chen QL, Sun LD, Hu W (2013) Molecular cloning and expression pattern of 11 genes involved in lipid metabolism in yellow catfish Pelteobagrus fulvidraco. Gene 53:53–63

    Google Scholar 

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Funding

The work was financially supported by Guangdong Marine Economy Promotion Projects (MEPP) Fund (GDOE [2019] A26), Guangdong Provincial Special Fund For Modern Agriculture Industry Technology Innovation Teams (2019KJ150), Department of Agriculture and Rural Affairs of Guangdong Province, Guangdong Forestry Science Technology and Innovation Commission (2018KJCX001), and Project of Department of Ocean and Fishery of Guangdong Province, China (A201701C03).

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  1. Shi-Jun Chen and Peng Liu contributed equally to this work.

Authors and Affiliations

  1. College of Marine Sciences, South China Agricultural University, Guangzhou, 510642, People’s Republic of China

    Shi-Jun Chen, Peng Liu, You-Ming Jia, Hong-Ping Liao, Shao-Xuan Zhu, Li-Liu Zhou, Xue-Ming Dan, Li Liu & Lian Gan

  2. Guangdong Laboratory for Lingnan Modern Agriculture, South China Agricultural University, Guangzhou, 510642, People’s Republic of China

    Shi-Jun Chen, Peng Liu, You-Ming Jia, Hong-Ping Liao, Shao-Xuan Zhu, Li-Liu Zhou, Xue-Ming Dan, Li Liu & Lian Gan

  3. Foshan DBN Huilin Aquaculture Science & Technology Co. Ltd, Foshan, 524500, People’s Republic of China

    Jia-Hao Li, Su-Bi Zheng & Jun-Jiang Yang

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  1. Shi-Jun Chen
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Correspondence to Lian Gan.

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All procedures implemented for fish followed the handling guidelines of South China Agricultural University.

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Chen, SJ., Liu, P., Jia, YM. et al. Dietary lipid concentrations influence growth, body composition, morphology of the liver and mid-intestine, and antioxidant status of marbled eel (Anguilla marmorata). Aquacult Int 28, 2287–2302 (2020). https://doi.org/10.1007/s10499-020-00590-5

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