Effects of Dietary Carbohydrate Level on Growth Performance, Body Composition, Plasma Biochemical Parameters and Intestinal and Liver Enzyme Activities of Orange-Spotted Grouper (Epinephelus coioides)

LIU Hao; YANG Junjiang; DONG Xiaohui; TAN Beiping; YANG Qihui; CHI Shuyan; LIU Hongyu; ZHANG Shuang; YANG Yuanzhi

doi:10.3969/j.issn.1006-267x.2020.01.042

2020 , Vol. 32 >Issue 1: 357 - 371

DOI: https://doi.org/10.3969/j.issn.1006-267x.2020.01.042

Effects of Dietary Carbohydrate Level on Growth Performance, Body Composition, Plasma Biochemical Parameters and Intestinal and Liver Enzyme Activities of Orange-Spotted Grouper (Epinephelus coioides)

LIU Hao ,
YANG Junjiang ,
DONG Xiaohui ,
TAN Beiping ,
YANG Qihui ,
CHI Shuyan ,
LIU Hongyu ,
ZHANG Shuang ,
YANG Yuanzhi

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1. Laboratory of Aquatic Animal Nutrition and Feed, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China;
2. Aquatic Animals Precision Nutrition and High-Efficiency Feed Engineering Research Center of Guangdong Province, Zhanjiang 524088, China

Received date: 2019-06-24

Online published: 2020-01-19

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Abstract

This experiment was conducted to explore the effects of dietary carbohydrate level on growth performance, body composition, plasma biochemical parameters and intestinal and liver enzyme activities of orange-spotted grouper (Epinephelus coioides). A total of 300 healthy orange-spotted grouper with initial weight of (102.80±1.02) g were randomly divided into 5 groups with 3 replicates per group and 20 fish per replicate. Fish in 5 groups were fed isonitrogenous and isoenergetic experimental diets which carbohydrate levels were 7%, 14%, 21%, 28% and 35%, respectively. The experiment lasted for 810 weeks. The results showed as follows:1) the specific growth rate (SGR) and weight gain rate (WGR) of 28% group were significantly higher than those of other groups (P<0.05), the feed conversion ratio (FCR) of 28% group was significantly lower than that of 7% and 14% group (P<0.05), the protein efficiency ratio (PER), condition factor (CF) and hepatosomatic index (HSI) of 28% and 35% groups were significantly higher than those of 7% group (P<0.05), and the viscerosomatic index (VSI) of 35% group was significantly higher than that of 7% group (P<0.05). 2) The apparent digestibility of dry matter of 7% group was significantly lower than that of 21%, 28% and 31% groups (P<0.05), and the apparent digestibilities of crude lipid and energy of 35% groups were significantly lower than those of 7%, 14% and 21% groups (P<0.05). 3) The whole body crude protein content of 28% and 35% groups was significantly lower than that of 7% group (P<0.05), the whole body crude lipid content of 35% group was significantly higher than that of other groups (P<0.05), and the whole body ash content of 35% group was significantly lower than that of 7%, 14% and 28% groups (P<0.05). The muscle crude lipid content of 28% and 35% groups was significantly higher than that of 7% group (P<0.05), and the muscle ash content of 7% group was significantly higher than that of other groups (P<0.05). The liver glycogen content of 35% group was significantly higher than that of 7%, 14% and 21% groups (P<0.05), and the muscle glycogen content of 35% group was significantly higher than that of other groups (P<0.05). 4) The plasma total protein (TP) content of 7% group was significantly lower than that of other groups (P<0.05), the plasma glucose (GLU) content of 21%, 28% and 35% groups was significantly higher than that of 7% and 14% groups (P<0.05), the plasma triglyceride (TG) content of 28% and 35% groups was significantly higher than that of 7% and 14% groups (P<0.05), and the plasma total cholesterol (TC) content of 28% and 35% groups was significantly higher than that of 7%, 14% and 21% groups (P<0.05). 5) The liver hexokinase (HK) activity of 35% group was significantly higher than that of 7% group (P<0.05), the liver phosphofructokinase (PFK) activity of 35% group was significantly higher than that of other groups (P<0.05), the liver glucose-6-phosphate dehydrogenase (G6PDH) activity of 35% group was significantly higher than that of 7%, 14% and 21% groups (P<0.05), and the liver fructos-1,6-diphosphatase (FBPase) activity of 21% and 28% group was significantly higher than that of 7%, 14% and 38% groups (P<0.05). 6) The intestinal pepsin (PS) activity of 35% group was significantly higher than that of 7%, 14% and 28% groups (P<0.05), the intestinal lipase (LPS) activity of 35% group was significantly lower than that of 7%, 14% and 28% groups (P<0.05), and the intestinal amylase (AMS) activity of 35% group was significantly higher than that of 7%, 14% and 28% groups (P<0.05). 7) The liver alkaline phosphatase (AKP) activity of 35% group was significantly higher than that of other groups (P<0.05), the liver acid phosphatase (ACP) activity of 7% group was significantly higher than that of 21%, 28% and 35% groups (P<0.05), the liver superoxide dismutase (SOD) activity of 28% group was significantly higher than that of 7% group (P<0.05), and the liver lysozyme (LZM) activity of 28% and 35% groups was significantly higher than that of 7%, 14% and 21% groups (P<0.05). In conclusion, dietary suitable carbohydrate level can improve the growth performance of orange-spotted grouper, and has a certain impact on body composition, nutrient apparent digestibility, plasma biochemical parameters and activities of digestive, immune and metabolic enzymes, dietary high carbohydrate level will cause the rise of HSI, VSI and contents of liver glycogen, muscle glycogen of fish. Using SGR as the evaluation index, the quadratic regression curve model shows that the optimal dietary carbohydrate requirement for orange-spotted grouper is 28.50%.

Key words： Epinephelus coioides; carbohydrate level; growth performance; plasma biochemical parameters; liver immune enzyme; intestinal digestive enzyme

Cite this article

LIU Hao , YANG Junjiang , DONG Xiaohui , TAN Beiping , YANG Qihui , CHI Shuyan , LIU Hongyu , ZHANG Shuang , YANG Yuanzhi . Effects of Dietary Carbohydrate Level on Growth Performance, Body Composition, Plasma Biochemical Parameters and Intestinal and Liver Enzyme Activities of Orange-Spotted Grouper (Epinephelus coioides)[J]. Chinese Journal of Animal Nutrition, 2020 , 32(1) : 357 -371 . DOI: 10.3969/j.issn.1006-267x.2020.01.042

References

[1] WILSON R P.Utilization of dietary carbohydrate by fish[J].Aquaculture,1994,124(1/2/3/4):67-80.
[2] 刘泓宇,毛义波,谭北平,等.饲料糖水平对不同食性鱼类生长及葡萄糖耐受能力的影响[J].水产学报,2015,39(12):1852-1862.
[3] 李晓宁.饲料糖水平对大菱鲆和牙鲆生长、生理状态参数及体组成的影响[D].硕士学位论文.青岛:中国海洋大学,2011.
[4] SHIAU S Y.Utilization of carbohydrates in warmwater fish-with particular reference to tilapia,Oreochromis niloticus×O. aureus[J].Aquaculture,1997,151(1/2/3/4):79-96.
[5] GARCÍA-GALLEGO M,BAZOCO J,SUÀREZ M D,et al.Utilization of dietary carbohydrates by fish:a comparative study in eel and trout[J].Animal Science,1995,61(2):427-436.

[6] LIN J H,SHIAU S Y.Hepatic enzyme adaptation to different dietary carbohydrates in juvenile tilapia Oreochromis niloticus×O. aureus[J].Fish Physiology and Biochemistry,1995,14(2):165-170.

[7] NRC.Nutrient requirements of fish and shrimp[S].Washington,D.C.:National Academies Press,2011.
[8] HUTCHINS C G,RAWLES S D,GATLIN Ⅲ D M.Effects of dietary carbohydrate kind and level on growth,body composition and glycemic response of juvenile sunshine bass (Morone chrysops ♀×M. saxatilis♂)[J].Aquaculture,1998,161(1/2/3/4):187-199.
[9] BERGOT F.Effects of dietary carbohydrates and of their mode of distribution on glycaemia in rainbow trout (Salmo gairdneri Richardson)[J].Comparative Biochemistry and Physiology Part A:Physiology,1979,64(4):543-547.

[10] LIN S M,SHI C M,MU M M,et al.Effect of high dietary starch levels on growth,hepatic glucose metabolism,oxidative status and immune response of juvenile largemouth bass,Micropterus salmoides[J].Fish & Shellfish Immunology,2018,78:121-126.
[11] MA H J,MOU M M,PU D C,et al.Effect of dietary starch level on growth,metabolism enzyme and oxidative status of juvenile largemouth bass,Micropterus salmoides[J].Aquaculture,2019,498:482-487.
[12] PERES H,GONÇALVES P,OLIVA-TELES A.Glucose tolerance in gilthead seabream (Sparus aurata) and European seabass (Dicentrarchus labrax)[J].Aquaculture,1999,179(1/2/3/4):415-423.
[13] BORREBAEK B,CHRISTOPHERSEN B.Hepatic glucose phosphorylating activities in perch (Perca fluviatilis) after different dietary treatments[J].Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology,2000,125(3):387-393.

[14] DENG D F,REFSTIE S,HUNG S S O.Glycemic and glycosuric responses in white sturgeon (Acipenser transmontanus) after oral administration of simple and complex carbohydrates[J].Aquaculture,2001,199(1/2):107-117.
[15] WU C L,YE J Y,GAO J E,et al.Effect of varying carbohydrate fractions on growth,body composition,metabolic,and hormonal indices in juvenile black carp,Mylopharyngodon piceus[J].Journal of the World Aquaculture Society,2016,47(3):435-449.

[16] XIA S L,LI X F,ABASUBONG K P,et al.Effects of dietary glucose and starch levels on the growth,apparent digestibility,and skin-associated mucosal non-specific immune parameters in juvenile blunt snout bream (Megalobrama amblycephala)[J].Fish & Shellfish Immunology,2018,79:193-201.
[17] GARCIA GALLEGO M,HIDALGO M C,SUAREZ M D,et al.Feeding of the european eel Anguilla anguilla Ⅱ.Influence of dietary lipid level[J].Comparative Biochemistry and Physiology Part A:Physiology,1993,105(1):171-175.

[18] DEGANI G,VIOLA S.The protein sparing effect of carbohydrates in the diet of eels (Anguilla anguilla)[J].Aquaculture,1987,64(4):283-291.

[19] PERAGÍN J,BARROSO J B,GARCÍA-SALGUERO L,et al.Carbohydrates affect protein-turnover rates,growth,and nucleic acid content in the white muscle of rainbow trout (Oncorhynchus mykiss)[J].Aquaculture,1999,179(1/2/3/4):425-437.
[20] SUAREZ R K,MOMMSEN T P.Gluconeogenesis in teleost fishes[J].Canadian Journal of Zoology,1987,65(8):1869-1882.

[21] 裴之华,解绶启,雷武,等.长吻鮠和异育银鲫对玉米淀粉利用差异的比较研究[J].水生生物学报,2005,29(3):239-246.
[22] HEMRE G I,SANDNES K,LIE Ø,et al.Carbohydrate nutrition in Atlantic salmon,Salmo salar L.:growth and feed utilization[J].Aquaculture Research,1995,26(3):149-154.

[23] WANG J T,LI X Y,HAN T,et al.Effects of different dietary carbohydrate levels on growth,feed utilization and body composition of juvenile grouper Epinephelus akaara[J].Aquaculture,2016,459:143-147.
[24] WANG Y,LIU Y J,TIAN L X,et al.Effects of dietary carbohydrate level on growth and body composition of juvenile tilapia,Oreochromis niloticus×O. aureus[J].Aquaculture Research,2005,36(14):1408-1413.

[25] WU C L,YE J Y,GAO J E,et al.The effects of dietary carbohydrate on the growth,antioxidant capacities,innate immune responses and pathogen resistance of juvenile Black carp Mylopharyngodon piceus[J].Fish & Shellfish Immunology,2016,49:132-142.
[26] SUWIRYA K,GIRI N A,MARZUQI M,et al.Utilisation of dietary dextrin by juvenile humpback grouper (Cromileptes altivelis)[C]//RIMMER M A,MCBRIDE S,WILLIAMS K C.Advances in grouper acquaculture.Canberra:Australian Centre for International Agricultural Research,2004:107-109.
[27] LI S L,LI Z Q,CHEN N S,et al.Dietary lipid and carbohydrate interactions:implications on growth performance,feed utilization and non-specific immunity in hybrid grouper (Epinephelus fuscoguttatus ♀×E. lanceolatus♂)[J].Aquaculture,2019,498:568-577.
[28] 王勇.斜带石斑鱼利用糖的研究及与杂交罗非鱼的比较[D].博士学位论文.广州:中山大学,2006.
[29] AOAC.Official methods of analysis[S].Arlington,VA:Association of Official Analytical Chemists,1995.
[30] CHENG Z Y,AI Q H,MAI K S,et al.Effects of dietary canola meal on growth performance,digestion and metabolism of Japanese seabass,Lateolabrax japonicus[J].Aquaculture,2010,305(1/2/3/4):102-108.
[31] ELLIS A E.Lysozyme assay[C]//STOLEN J S,FLETCHER T C,ANDERSON B S,et al.Techniques in fish immunology.Fair Haven,NJ:SOS Publications,1990.
[32] WEBER J M,HAMAN F.Pathways for metabolic fuels and oxygen in high performance fish[J].Comparative Biochemistry and Physiology Part A:Physiology,1996,113(1):33-38.

[33] 黄岩,李建,王学习,等.饲料中不同蛋白质和淀粉水平对斜带石斑鱼生长性能和肝脏相关代谢酶活性的影响[J].水产学报,2017,41(5):746-756.
[34] REN M C,HABTE-TSION H M,XIE J,et al.Effects of dietary carbohydrate source on growth performance,diet digestibility and liver glucose enzyme activity in blunt snout bream,Megalobrama amblycephala[J].Aquaculture,2015,438:75-81.
[35] LEE S M,PARK C S,BANG I C.Dietary protein requirement of young Japanese flounder Paralichthys olivaceus fed isocaloric diets[J].Fisheries Science,2002,68(1):158-164.

[36] LIU X H,YE C X,ZHENG L M,et al.Dietary maize starch influences growth performance,apparent digestibility coefficient,and hepatic enzyme activities of carbohydrate metabolism in obscure puffer,Takifugu obscurus (Abe)[J].Journal of the World Aquaculture Society,2015,46(1):102-113.

[37] REN M C,AI Q H,MAI K S,et al.Effect of dietary carbohydrate level on growth performance,body composition,apparent digestibility coefficient and digestive enzyme activities of juvenile cobia,Rachycentron canadum L[J].Aquaculture Research,2011,42(10):1467-1475.

[38] MOREIRA I S,PERES H,COUTO A,et al.Temperature and dietary carbohydrate level effects on performance and metabolic utilisation of diets in European sea bass (Dicentrarchus labrax) juveniles[J].Aquaculture,2008,274(1):153-160.

[39] XIA B,GAO Q F,WANG J Y,et al.Effects of dietary carbohydrate level on growth,biochemical composition and glucose metabolism of juvenile sea cucumber Apostichopus japonicus (Selenka)[J].Aquaculture,2015,448:63-70.
[40] 赵永志.青鱼对饲料糖的利用[D].硕士学位论文.苏州:苏州大学,2009.
[41] CHENG Z Y,MAI K S,AI Q H,et al.Effects of dietary pregelatinized corn starch on growth,apparent digestibility,and digestive enzyme activity of large yellow croaker fingerlings (Pseudosciaena crocea)[J].Israeli Journal of Aquaculture-Bamidgeh,2013,65(1):843-850.
[42] BOONANUNTANASARN S,KUMKHONG S,YOOHAT K,et al.Molecular responses of Nile tilapia (Oreochromis niloticus) to different levels of dietary carbohydrates[J].Aquaculture,2018,482:117-123.
[43] BRAUGE C,CORRAZE G,MEDALE F.Combined effects of dietary lipid carbohydrate ratio and environmental factors on growth and nutritional balance in rainbow trout[J].From discovery to commercialization,1993:209.
[44] GOUVEIA A,OLIVA-TELES A,GOMES E,et al.The effect of two dietary levels of raw and gelatinized starch on growth and food utilization by the European seabass[C]//Proceedings of actas del V congresso nacional de acuicultura.Barcelona:Universitat de Barcelona,1995:516-521.
[45] MOHANTA K N,MOHANTY S N,JENA J,et al.Carbohydrate level in the diet of silver barb,Puntius gonionotus (Bleeker) fingerlings:effect on growth,nutrient utilization and whole body composition[J].Aquaculture Research,2009,40(8):927-937.

[46] 蒋湘辉,刘刚,金广海,等.饲料蛋白质和能量水平对草鱼生长和鱼体组成的影响[J].水产学杂志,2010,23(1):24-27.
[47] 胡毅,陈云飞,张德洪,等.不同碳水化合物和蛋白质水平膨化饲料对大规格草鱼生长、肠道消化酶及血清指标的影响[J].水产学报,2018,42(5):777-786.
[48] KEEMBIYEHETTY C N,WILSON R P.Effect of water temperature on growth and nutrient utilization of sunshine bass (Morone chrysops ♀×Morone saxatilis♂) fed diets containing different energy/protein ratios[J].Aquaculture,1998,166(1/2):151-162.
[49] ABDEL-TAWWAB M,AHMAD M H,KHATTAB Y A E,et al.Effect of dietary protein level,initial body weight,and their interaction on the growth,feed utilization,and physiological alterations of Nile tilapia,Oreochromis niloticus (L.)[J].Aquaculture,2010,298(3/4):267-274.
[50] TIAN L X,LIU Y J,YANG H J,et al.Effects of different dietary wheat starch levels on growth,feed efficiency and digestibility in grass carp (Ctenopharyngodon idella)[J].Aquaculture International,2012,20(2):283-293.

[51] CASTRO C,PERÉZ-JIMÉNEZ A,COUTINHO F,et al.Dietary carbohydrate and lipid sources affect differently the oxidative status of European sea bass (Dicentrarchus labrax) juveniles[J].British Journal of Nutrition,2015,114(10):1584-1593.

[52] KAMALAM B S,MÉDALE F,LARROQUET L,et al.Metabolism and fatty acid profile in fat and lean rainbow trout lines fed with vegetable oil:effect of carbohydrates[J].PLoS One,2013,8(10):e76570.
[53] LU S D,WU X Y,GAO Y J,et al.Effects of dietary carbohydrate sources on growth,digestive enzyme activity,gene expression of hepatic GLUTs and key enzymes involved in glycolysis-gluconeogenesis of giant grouper Epinephelus lanceolatus larvae[J].Aquaculture,2018,484:343-350.
[54] LI J N,XU Q Y,WANG C A,et al.Effects of dietary glucose and starch levels on the growth,haematological indices and hepatic hexokinase and glucokinase mRNA expression of juvenile mirror carp (Cyprinus carpio)[J].Aquaculture Nutrition,2016,22(3):550-558.

[55] KIRCHNER S,SEIXAS P,KAUSHIK S et al.Effects of low protein intake on extra-hepatic gluconeogenic enzyme expression and peripheral glucose phosphorylation in rainbow trout (Oncorhynchus mykiss)[J].Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology,2005,140(2):333-340.

[56] SHIAU S Y,CHEN M J.Carbohydrate utilization by tilapia (Oreochromis niloticus×O.aureus) as influenced by different chromium sources[J].The Journal of Nutrition,1993,123(10):1747-1753.

[57] FERNÁNDEZ F,MIQUEL A G,CÍRDOBA M,et al.Effects of diets with distinct protein-to-carbohydrate ratios on nutrient digestibility,growth performance,body composition and liver intermediary enzyme activities in gilthead sea bream (Sparus aurata,L.) fingerlings[J].Journal of Experimental Marine Biology and Ecology,2007,343(1):1-10.

[58] ENES P,PANSERAT S,KAUSHIK S,et al.Growth performance and metabolic utilization of diets with native and waxy maize starch by gilthead sea bream (Sparus aurata) juveniles[J].Aquaculture,2008,274(1):101-108.

[59] 王渊源,孙微涛.鱼虾需要的碳水化合物[J].福建水产,1992(3):87-92.
[60] ENES P,PANSERAT S,KAUSHIK S,et al.Effect of normal and waxy maize starch on growth,food utilization and hepatic glucose metabolism in European sea bass (Dicentrarchus labrax) juveniles[J].Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology,2006,143(1):89-96.

[61] KIRCHNER S,KAUSHIK S,PANSERAT S.Low protein intake is associated with reduced hepatic gluconeogenic enzyme expression in rainbow trout (Oncorhynchus mykiss)[J].The Journal of Nutrition,2003,133(8):2561-2564.

[62] ENES P,PANSERAT S,KAUSHIK S,et al.Nutritional regulation of hepatic glucose metabolism in fish[J].Fish Physiology and Biochemistry,2009,35(3):519-539.

[63] BARROSO J B,PERAGÍN J,GARCÍA-SALGUERO L,et al.Carbohydrate deprivation reduces NADPH-production in fish liver but not in adipose tissue[J].The International Journal of Biochemistry & Cell Biology,2001,33(8):785-796.

[64] SUÁREZ M D,HIDALGO M C,GARCÍA GALLEGO M,et al.Influence of the relative proportions of energy yielding nutrients on liver intermediary metabolism of the European eel[J].Comparative Biochemistry and Physiology Part A:Physiology,1995,111(3):421-428.

[65] SHIMENO S,SHIKATA T.Effects of acclimation temperature and feeding rate on carbohydrate-metabolizing enzyme activity and lipid content of common carp[J].Nippon Suisan Gakkaishi,1993,59(4):661-666.

[66] FERNÁNDEZ I,MOYANO F J,DÍAZ M,et al.Characterization of α-amylase activity in five species of mediterranean sparid fishes (Sparidae,Teleostei)[J].Journal of Experimental Marine Biology and Ecology,2001,262(1):1-12.

[67] MOHAMMADZADEH S,NOVERIAN H A,OURAJI H,et al.Growth,body composition and digestive enzyme responses of Caspian Kutum,Rutilus frisii (Kamenskii,1901),juveniles fed different levels of carbohydrates[J].Journal of Applied Ichthyology,2017,33(5):983-990.

[68] RIBEIRO L,ZAMBONINO-INFANTE J L,CAHU C,et al.Digestive enzymes profile of Solea senegalensis post larvae fed Artemia and a compound diet[J].Fish Physiology and Biochemistry,2002,27(1/2):61-69.

[69] NATALIA Y,HASHIM R,ALI A,et al.Characterization of digestive enzymes in a carnivorous ornamental fish,the Asian bony tongue Scleropages formosus (Osteoglossidae)[J].Aquaculture,2004,233(1/2/3/4):305-320.
[70] HEMRE G I,HANSEN T.Utilisation of different dietary starch sources and tolerance to glucose loading in Atlantic salmon (Salmo salar),during parr-smolt transformation[J].Aquaculture,1998,161(1/2/3/4):145-157.
[71] HEMRE G I,DENG D F.Carbohydrates[C]//Dietary nutrients,additives,and fish health.Hoboken,NJ:John Wiley & Sons,Inc,2015:95-110.
[72] ENES P,SANCHEZ-GURMACHES J,NAVARRO I,et al.Role of insulin and IGF-Ⅰ on the regulation of glucose metabolism in European sea bass (Dicentrarchus labrax) fed with different dietary carbohydrate levels[J].Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology,2010,157(4):346-353.

[73] ZHOU C P,GE X P,LIN H Z,et al.Effect of dietary carbohydrate on non-specific immune response,hepatic antioxidative abilities and disease resistance of juvenile golden pompano (Trachinotus ovatus)[J].Fish & Shellfish Immunology,2014,41(2):183-190.

[74] BARTON B A,IWAMA G K.Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids[J].Annual Review of Fish Diseases,1991,1:3-26.
[75] 杜启艳,王萍,王友利,等.长期饥饿和再投喂对泥鳅不同组织糖原、酸性磷酸酶和碱性磷酸酶的影响[J].江西师范大学学报(自然科学版),2008,32(4):488-493.

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