Chinese Journal of Animal Nutrition >

2024 , Vol. 36 >Issue 3: 1782 - 1794

DOI: https://doi.org/10.12418/CJAN2024.156

RESEARCH PAPER

Effects of Replacement of Fish Meal with Fermented Fish Processing Wastes on Growth, Hepatic Antioxidant Ability and Intestinal Structure of Juvenile Largemouth Bass (Micropterus salmoides)

  • WANG Yuyu , 1 ,
  • FU Ning 1 ,
  • AN Meiling 1 ,
  • ZHANG Yongming 1 ,
  • CUI Kai 2 ,
  • ZHANG Yongqin 3 ,
  • GUO Xiaohua 3 ,
  • WANG Junxia 4 ,
  • GUO Jianjun , 4, *
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  • 1 Department of Marine Technology, Rizhao Polytechnic, Rizhao 276826, China
  • 2 Anhui Province Key Laboratory of Aquaculture & Stock Enhancement, Hefei 230031, China
  • 3 Shandong Meijia Group Co., Ltd., Rizhao 276800, China
  • 4 Rizhao Ocean and Fisheries Institution, Rizhao 276800, China
*senior engineer, E-mail:

Received date: 2023-10-10

  Online published: 2024-03-13

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Abstract

A 10-week feeding trial was conducted in indoor culture system to evaluate effects of replacement of fish meal with fermented fish processing wastes (FFPW) on growth, serum biochemical indices, hepatic antioxidant ability and intestinal structure of juvenile largemouth bass [initial body weight: (5.87±0.04) g]. Four isonitrogenous diets were formulated to replace fish meal by FFPW at 0 (FFPW0), 10% (FFPW10), 20% (FFPW20) and 40% (FFPW40), respectively. A total of 360 fish with similar size were randomly allotted to 4 groups, each group consisted of three replicates with 30 fish per replicate, and three tanks of fish were fed for each diet. These results showed that compared with FFPW0 group, replacing 10% to 40% of fish meal with FFPW had no significant effects on survival rate, final body weight, weight gain rate and specific growth rate (P>0.05), however, the final body weight, weight gain rate and specific growth rate in FFPW20 group were significantly higher than those in FFPW40 group (P<0.05), but no significant difference was observed between FFPW20 group and FFPW10 group (P>0.05). Replacing 10% to 40% of fish meal with FFPW had no significant effects on feeding intake, feed coefficient, protein efficiency ratio, condition factor and viscerosomatic index (P>0.05). Fish in FFPW20 group had significantly higher hepatosomatic index than those in FFPW0 and FFPW40 groups (P<0.05). Fish in FFPW20 group had the lowest moisture and crude protein contents of whole body and the highest crude lipid content. The muscle crude lipid content was significantly lower in FFPW0 group than that in FFPW20 and FFPW40 groups (P<0.05). Muscle moisture content in FFPW0 group was significantly higher than that in FFPW replacement groups (P<0.05). With the increase of FFPW replacement level, serum total protein content was gradually increased, while serum glucose and triglyceride contents were gradually decreased, especially the FFPW40 group changed significantly (P<0.05). Replacing 10% to 40% of fish meal with FFPW had no significant effect on hepatic antioxidant enzyme and intestinal digestive enzyme activities (P>0.05). The villus length in FFPW0 group was significantly higher than that in FFPW replacement group (P<0.05), while the thickness of muscular layer was significantly lower than that in FFPW40 group (P<0.05). In conclusion, under the experimental conditions, 40% of fish meal can be replaced by FFPW for juvenile largemouth bass without having a negative effect on growth, feed utilization, antioxidant and immunity, and intestinal health.

Key words： largemouth bass; fish meal; fermented fish processing wastes; growth; intestinal structure

Cite this article

WANG Yuyu , FU Ning , AN Meiling , ZHANG Yongming , CUI Kai , ZHANG Yongqin , GUO Xiaohua , WANG Junxia , GUO Jianjun . Effects of Replacement of Fish Meal with Fermented Fish Processing Wastes on Growth, Hepatic Antioxidant Ability and Intestinal Structure of Juvenile Largemouth Bass (Micropterus salmoides)[J]. Chinese Journal of Animal Nutrition, 2024 , 36(3) : 1782 -1794 . DOI: 10.12418/CJAN2024.156

鱼粉因其适口性好、营养价值高和消化率高而被广泛用作水产饲料的动物蛋白质源[1]。鱼粉的用量和质量在很大程度上决定了水产饲料的质量和养殖效益。然而,由于过度捕捞和环境污染等引起海洋渔业资源衰减,据估计,鱼粉产量未来将会维持在年产500万t左右,而水产养殖业的增长对鱼粉的需求越来越大,这种供求关系的不平衡导致鱼粉价格飙升,进而增加饲料和养殖成本,从而严重制约水产养殖业的发展[2]。因此,在保证鱼类正常生长、健康和产品品质的前提下,急切需要寻找能够部分甚至完全替代鱼粉的蛋白质源,以节约饲料成本,提高养殖效益。
我国每年产生1 000万~1 800万t水产品加工副产物,其中,鱼头、鱼骨、鱼鳞、鱼皮、内脏和碎肉等占原料鱼体质量的40%~55%[3]。水产加工副产物富含蛋白质、胶原蛋白、必需氨基酸、多不饱和脂肪酸、类胡萝卜素、矿物质和生物活性成分等,具有极高的利用价值,但是其不易储存,易氧化酸败,会造成严重的环境污染[4⇓-6]。目前,水产加工副产物大多用于生产低值鱼粉,这造成了资源的极大浪费。如何充分利用水产加工副产物这一廉价蛋白质源是解决饲料蛋白质原料短缺的重要途径之一,也是科研工作者和整个饲料行业关注的焦点。豆粕被认为是水产饲料中替代鱼粉的优质植物蛋白质源之一,但是其适口性差、含有抗营养因子、必需氨基酸不平衡的缺点限制了其在水产饲料中的使用量[7]。
发酵被认为是提高动物和植物蛋白质源营养价值的重要手段之一。利用微生物发酵可将蛋白质源中对动物有毒有害的物质或不能完全消化吸收的物质进行降解,从而产生易被动物消化吸收的蛋白质、活性肽和游离氨基酸以及有机酸和酶类等,从而提高蛋白质源的营养价值[8⇓-10]。研究结果显示,微生物固态发酵水产加工副产物和植物蛋白质源适量替代鱼粉时,可补充鱼虾类所需游离氨基酸和不饱和脂肪酸等营养素以及多肽、乳酸等生物活性成分、平衡饲料氨基酸组成、降低饲料成本、减少环境污染[10⇓⇓-13]。因此,将水产品加工副产物加入到循环经济的产业链中,具有广阔的应用前景。
大口黑鲈具有生长快、肉质鲜美、无肌间刺和适应性强等优点,深受消费者和养殖者青睐,已成为我国重要的淡水养殖鱼类之一[14]。据中国渔业统计年鉴数据,2022年大口黑鲈养殖总产量为80.2万t,占淡水鱼类养殖产量的2.96%[15]。目前,大口黑鲈配合饲料中鱼粉用量达40%~54%,导致养殖成本过高[16]。截至目前,鲜见发酵鲭鱼加工副产物(FFPW)在大口黑鲈饲料中应用的相关研究报道。因此,本试验以大口黑鲈幼鱼[(5.87±0.04) g]为试验对象,研究FFPW替代鱼粉对大口黑鲈幼鱼生长、饲料利用、体组成、血清生化指标、肝脏抗氧化能力及消化酶活性、肠道健康等方面的影响,以期为大口黑鲈幼鱼配合饲料中FFPW的合理应用提供技术支持,促进大口黑鲈养殖业绿色健康发展。

1 材料与方法

1.1 试验饲料

以鱼粉为主要蛋白质源,鱼油为脂肪源,辅以酵母、血粉、玉米蛋白粉、维生素预混料、矿物质预混料、胆碱、磷脂等原料,配制基础饲料。FFPW由山东某集团有限公司提供,是由鲭鱼加工副产物与豆粕按照1∶1比例混合,添加植物乳杆菌、枯草芽孢杆菌和酿酒酵母等固态发酵而成,活菌数6.7×108 CFU/g。FFPW中粗蛋白质和粗脂肪含量分别为45.20%和12.01%。以FFPW分别替代基础饲料(FFPW0)中10%、20%和40%的鱼粉,分别标记为FFPW10、FFPW20和FFPW40,配制4种等氮等能试验饲料。饲料组成及营养水平见表1。饲料氨基酸组成见表2。
表1 饲料组成及营养水平(干物质基础)

Table 1 Composition and nutrient levels of diets (DM basis) %

项目
Items		 组别 Groups
FFPW0 FFPW10 FFPW20 FFPW40
原料 Ingredients
鱼粉 Fish meal 50.00 45.00 41.00 32.00
发酵鲭鱼加工副产物 FFPW 7.27 14.54 29.07
酵母 Beer yeast 3.00 3.00 3.00 3.00
玉米蛋白 Corn gluten 5.00 5.00 5.00 5.00
喷雾干燥血粉 Spray-dried blood meal 5.00 5.00 5.00 5.00
南极磷虾粉 Antarctic krill meal 10.00 10.00 10.00 10.00
面粉 Wheat meal 15.10 13.23 10.36 5.83
鱼油 Fish oil 6.00 5.60 5.20 4.20
维生素预混料 Vitamin premix1) 0.70 0.70 0.70 0.70
矿物质预混料 Mineral premix2) 0.70 0.70 0.70 0.70
胆碱 Choline 0.50 0.50 0.50 0.50
磷脂 Phospholipids 1.50 1.50 1.50 1.50
磷酸二氢钙 Ca(H2PO4)2 1.00 1.00 1.00 1.00
低聚糖 Oligosaccharide 1.50 1.50 1.50 1.50
合计 Total 100.00 100.00 100.00 100.00
营养水平 Nutrient levels3)
粗蛋白质 Crude protein 50.38 49.30 50.30 50.18
粗脂肪 Crude lipid 11.64 11.90 12.31 11.20

1)维生素预混料为每千克饲料提供 Vitamin premix provided the following per kilogram of diets: VA 16 000 IU,VD3 8 000 IU,VE 160 mg,VK3 14.72 mg,VB1 17.80 mg,VB2 48 mg,VB6 29.52 mg,VB12 0.24 mg,烟酸 niacinamide 79.20 mg,泛酸钙 calcium pantothenate 73.60 mg,肌醇 inositol 320 mg,生物素 biotin 0.64 mg,叶酸 folic acid 6.40 mg,VC 800 mg。

2)矿物元素预混料为每千克饲料提供 Mineral premix provided the following per kilogram of diets: CoCl2 0.24 mg,FeSO4 21.10 mg,ZnSO4 34.4 mg,CuSO4 2.00 mg,MnSO4 6.20 mg,Ca (IO3)2 1.63 mg,Na2SeO3 0.18 mg。

3)实测值 measured values。

表2 饲料氨基酸组成(干物质基础)

Table 2 Composition of amino acids of diets (DM basis) %

氨基酸
Amino acids		 组别 Groups
FFPW0 FFPW10 FFPW20 FFPW40
必需氨基酸 EAA
精氨酸 Arg 2.55 2.53 2.54 2.70
组氨酸 His 1.39 1.37 1.29 1.41
异亮氨酸 Iso 1.83 1.85 1.88 2.04
亮氨酸 Leu 3.89 3.88 3.92 4.25
赖氨酸 Lys 2.98 3.00 3.02 3.22
蛋氨酸 Met 1.06 1.17 1.23 1.35
苯丙氨酸 Phe 2.05 2.08 2.10 2.29
苏氨酸 Thr 1.71 1.73 1.73 1.86
缬氨酸 Val 2.60 2.62 2.66 2.90
非必需氨基酸 NEAA
天冬氨酸 Asp 4.26 4.41 4.58 4.89
甘氨酸 Gly 2.43 2.55 2.81 3.09
谷氨酸 Glu 6.45 6.60 6.87 7.21
丙氨酸 Ala 2.93 3.06 3.20 3.47
丝氨酸 Ser 2.06 2.15 2.31 2.49
脯氨酸 Pro 3.35 3.40 3.56 3.87
半胱氨酸 Cys 0.59 0.56 0.61 0.65
酪氨酸 Tyr 1.82 1.98 2.11 2.24
配制饲料前,所有原料经过粉碎过60目筛。准确称量饲料原料,先将固体原料混合均匀,然后再加入鱼油和磷脂,手工将油脂颗粒搓细,混匀,最后添加30%水,再次混匀,双螺杆颗粒饲料机(河南郑州威龙机械,KL-210型)挤压成条状(粒径1.5 mm),60 ℃烘干,封口袋包装,-20 ℃保存备用。

1.2 养殖管理

养殖试验在日照职业技术学院水生物繁养殖实训中心循环水养殖系统中进行。试验用大口黑鲈幼鱼购自金澄福生物科技(苏州)有限公司,为当年人工孵化的同一批鱼苗。试验用鱼暂养于纤维玻璃钢养殖池(直径2 m,水深60 cm),采用基础饲料驯养2周,使其适应养殖环境和试验饲料。
试验在循环水养殖玻璃缸(1.00 m×0.45 m×0.45 m)中进行,试验开始前,试验鱼饥饿24 h。试验挑选出360尾健康无病、规格一致[(5.87±0.04) g]的幼鱼,随机为4个组,每组3个重复,每个重复30尾鱼。每种饲料随机投喂3缸鱼,每天饱饲投喂2次(08:00和17:00)。投喂前除去粪便等污物。整个养殖期间,水流量0.3 L/min,温度为(25.0±0.5) ℃,溶解氧含量为6.5~7.2 mg/L,pH为7.8~8.2,氨氮含量低于0.15 mg/L,光照周期为12h L/12 h D。养殖试验持续10周。

1.3 样品收集

养殖结束后,试验鱼饥饿24 h,准确称每缸鱼总重,记录鱼总数;每缸随机取5尾鱼,测量体质量、体长,分离内脏团、肝脏并称重,计算肥满度、肝体比和脏体比;取肌肉、肠道和肝脏并保存于-20 ℃冰箱,分别用于测定肌肉成分、消化酶和抗氧化酶活性;每缸随机取3尾鱼,-20 ℃冰箱中保存,用于测定全鱼成分。每缸随机取5尾鱼,MS-222麻醉,尾静脉取血,4 ℃冰箱静置2 h,5 000 r/min离心10 min,取上清液,-20 ℃保存。每缸选取3尾鱼,分离肠道并固定于4%多聚甲醛,用于制作肠道切片。

1.4 分析方法

体成分的测定:分别采用凯氏定氮法、索氏抽提法、灼烧法和烘干恒重法测定饲料、全鱼和肌肉中粗蛋白质(GB/T 6432—2018)、粗脂肪(GB/T 6433—2006)、粗灰分(GB/T 6438—2007)和水分(GB/T 6435—2014)含量。
血清生化指标的测定:采用全自动生化分析仪(迈瑞 BS-400, 深圳)测定血清谷丙转氨酶(ALT)、谷草转氨酶(AST)、碱性磷酸酶(ALP)活性及总蛋白(TP)、葡萄糖(GLU)、甘油三酯(TG)、总胆固醇(TC)和低密度脂蛋白(LDL)含量。
肝脏抗氧化指标的测定:将肝脏样品按照重量∶体积=1∶9的比例加入9倍体积的生理盐水,高速匀浆,然后于4 ℃,3 000 r/min,离心10 min,取上清液,用于测定总抗氧化能力(T-AOC)、过氧化氢酶(CAT)、总超氧化物气化酶(T-SOD)活性、丙二醛(MDA)含量,均采用南京建成生物工程研究所生产的试剂盒测定,具体测定过程参照试剂盒说明书。
肠道消化酶活性的测定:采用南京建成生物工程研究所生产的试剂盒测定肠道胰蛋白酶、α-淀粉酶和脂肪酶活性。
肠道组织切片:将固定好的肠道样品转入75%乙醇溶液中,进行乙醇梯度脱水,石蜡包埋,Leica RM2016型病理切片机切片(厚度为4 μm),苏木精-伊红染色,中性树胶封片。应用Image-Pro P1us 6.0分析软件测量绒毛长度、绒毛宽度和肌层厚度,并采用正置光学显微镜(Nikon Eclipse E100)拍照。

1.5 计算公式

成活率(SR,%)=100×(试验结束时尾数)/(试验开始时尾数);

增重率(WGR,%)=100×(鱼终末体重-鱼初始体重)/鱼初始体重;

特定生长率(SGR,%/d)=100×(ln鱼终末体重-ln鱼初始体重)/养殖周期;

饲料系数(FCR)=试验期间投料量/鱼净增重;

摄食率(FI, %/d)=100×试验期间投料量/[(鱼终末体重+鱼初始体重)/2×养殖周期];

蛋白质效率(PER)=鱼净增重/蛋白质摄取量;

肥满度(CF,g/cm3)=100×体重/体长3;

肝体比(HSI,%)=100×肝重/体重;

脏体比(VSI,%)=100×内脏重/体重。

1.6 统计分析

采用SPSS 21.0统计软件对数据进行统计学分析。先作单因素方差分析(one-way ANOVA),若各组之间差异显著,再作Duncan氏多重比较,P<0.05表示差异显著。试验结果采用“平均值±标准差”表示。

2 结果

2.1 FFPW替代鱼粉对大口黑鲈幼鱼生长、饲料效率和形态指数的影响

由表3可知,大口黑鲈幼鱼成活率为96.67%~100.00%,各组之间差异不显著(P>0.05)。与FFPW0组相比,FFPW替代10%~40%鱼粉对大口黑鲈终末体重、增重率和特定生长率无显著影响(P>0.05),FFPW20组显著高于FFPW40组(P<0.05),而与FFPW10组差异不显著(P>0.05);FFPW替代饲料中10%~40%鱼粉对摄食率、饲料系数、蛋白质效率、肥满度和脏体比无显著影响(P>0.05)。FFPW20组肝体比显著高于FFPW0组和FFPW40组(P<0.05),而与FFPW10组差异不显著(P>0.05)。
表3 FFPW替代鱼粉对大口黑鲈幼鱼生长、饲料效率和形态指数的影响

Table 3 Effects of replacement of fish meal with FFPW on growth, feed utilization and body indexes of juvenile largemouth bass

项目
Items		 组别 Groups
FFPW0 FFPW10 FFPW20 FFPW40
初始体重 IBW/g 5.86±0.03 5.87±0.04 5.88±0.02 5.87±0.07
终末体重 FBW/g 38.18±2.80ab 37.61±3.67ab 43.49±2.17b 36.55±1.07a
增重率 WGR/% 551.36±45.04ab 540.86±59.84ab 639.95±36.18b 523.18±20.71a
特定生长率 SGR/(%/d) 2.67±0.10ab 2.65±0.13ab 2.86±0.07b 2.61±0.05a
饲料系数 FCR 0.91±0.01 0.97±0.07 0.96±0.02 1.00±0.06
摄食率 FI/(%/d) 1.89±0.04 1.99±0.12 2.07±0.03 2.06±0.09
蛋白质效率 PER 2.18±0.03 2.11±0.16 2.07±0.04 2.00±0.11
成活率 SR/% 96.67±3.33 96.67±3.33 96.67±3.33 100.00±0.00
肥满度 CF/(g/cm3) 2.11±0.12 2.15±0.36 2.18±0.21 2.07±0.30
肝体比 HSI/% 1.09±0.27a 1.22±0.37ab 1.47±0.19b 1.08±0.22a
脏体比 VSI/% 6.77±0.21 6.64±0.27 6.89±0.14 7.14±0.20

同行数据肩标不同字母表示差异显著(P<0.05)。下表同。

Values in the same row with different letter superscripts mean significant difference (P<0.05). The same as below.

2.2 FFPW替代鱼粉对大口黑鲈幼鱼体成分的影响

由表4可知,FFPW替代鱼粉对大口黑鲈全鱼粗灰分、肌肉粗蛋白质和粗灰分含量影响不显著(P>0.05)。随着FFPW替代比例的升高,全鱼水分和粗蛋白质含量呈降低的趋势,尤其是FFPW20组,而全鱼粗脂肪含量的变化趋势正好相反。肌肉粗脂肪含量随FFPW替代比例的升高而逐渐升高,其中,FFPW0组显著低于FFPW20组和FFPW40组(P<0.05);FFPW0组肌肉水分含量显著高于FFPW替代组(P<0.05),FFPW替代组之间肌肉水分含量差异不显著(P>0.05)。
表4 FFPW替代鱼粉对大口黑鲈体成分的影响

Table 4 Effects of replacement of fish meal with FFPW on body composition of juvenile largemouth bass %

项目
Items		 组别 Groups
FFPW0 FFPW10 FFPW20 FFPW40
全鱼 Whole body
水分 Moisture 74.28±0.14b 72.88±0.36ab 71.82±0.86a 73.63±1.05ab
粗蛋白质 Crude protein 16.87±0.26b 16.61±0.23ab 16.76±0.15b 16.02±0.36a
粗脂肪 Crude lipid 4.94±0.17a 5.35±0.37ab 6.51±0.27b 5.20±0.43ab
粗灰分 Ash 3.81±0.10 3.90±0.27 4.04±0.08 3.99±0.09
肌肉 Muscle
水分 Moisture 77.21±0.23b 76.53±0.20a 75.99±0.23a 76.39±0.18a
粗蛋白质 Crude protein 19.36±0.22 20.30±0.56 19.58±0.06 19.82±0.69
粗脂肪 Crude lipid 1.40±0.10a 1.84±0.13ab 2.22±0.10b 2.02±0.32b
粗灰分 Ash 1.34±0.03 1.28±0.01 1.29±0.01 1.35±0.04

2.3 FFPW替代鱼粉对大口黑鲈幼鱼血清生化指标的影响

由表5可知,FFPW替代10%~40%鱼粉对血清ALT 、AST 、ALP活性及TC 、LDL含量无显著影响(P>0.05);随着FFPW替代比例的增加,血清TP含量逐渐升高,而血清GLU、TG含量逐渐降低,尤其是FFPW40组变化显著(P<0.05)。
表5 FFPW替代鱼粉对大口黑鲈幼鱼血清生化指标的影响

Table 5 Effects of replacement of fish meal with FFPW on serum biochemical indices of juvenile largemouth bass

项目
Items		 组别 Groups
FFPW0 FFPW10 FFPW20 FFPW40
谷丙转氨酶 ALT/(U/L) 3.35±0.39 3.89±0.60 3.51±0.66 3.26±0.62
谷草转氨酶 AST/(U/L) 6.05±0.83 5.86±0.60 5.68±0.77 6.63±0.90
碱性磷酸酶 ALP/(U/L) 58.66±3.90 62.33±2.89 61.51±2.73 60.55±3.17
总蛋白 TP/(g/L) 26.13±2.18a 26.50±2.05a 28.30±2.35ab 30.04±3.00b
葡萄糖 GLU/(mmol/L) 5.71±0.74b 5.18±0.46b 4.23±0.35a 3.62±0.78a
甘油三酯 TG/(mmol/L) 2.31±0.32b 2.17±0.14ab 2.22±0.30b 1.88±0.24a
总胆固醇 TC/(mmol/L) 5.02±0.47 4.76±0.85 4.99±0.97 4.83±0.75
低密度脂蛋白 LDL/(mmol/L) 1.44±0.15 1.33±0.19 1.32±0.17 1.24±0.15

2.4 FFPW替代鱼粉对大口黑鲈幼鱼肝脏抗氧化指标的影响

由表6可知,FFPW替代10%~40%鱼粉对肝脏T-SOD、CAT活性和T-AOC以及MDA含量无显著影响(P>0.05)。
表6 FFPW替代鱼粉对大口黑鲈幼鱼肝脏抗氧化指标的影响

Table 6 Effects of replacement of fish meal with FFPW on hepatic antioxidant indexes of juvenile largemouth bass

项目
Items		 组别 Groups
FFPW0 FFPW10 FFPW20 FFPW40
总超氧化歧化酶 T-SOD/(U/mg prot) 46.65±3.34 49.57±4.17 48.22±5.53 47.16±5.72
过氧化氢酶 CAT/(U/mg prot) 23.46±1.86 24.30±4.12 25.22±2.02 25.32±2.42
总抗氧化能力 T-AOC/(U/mg prot) 1.31±0.23 1.28±0.26 1.25±0.25 1.48±0.23
丙二醛 MDA/(nmol/mg prot) 1.23±0.26 1.17±0.19 1.32±0.12 1.26±0.20

2.5 FFPW替代鱼粉对大口黑鲈幼鱼肠道消化酶活性和肠道结构的影响

由表7可知,FFPW替代10%~40%鱼粉时,肠道脂肪酶、α-淀粉酶和胰蛋白酶活性有升高的趋势,但是差异不显著(P>0.05)。FFPW对肠道组织的影响结果显示,饲料中添加FFPW对肠道绒毛宽度影响不显著(P>0.05),FFPW0组鱼肠道绒毛长度显著高于FFPW替代组(P<0.05),而肌层厚度低于FFPW替代组(P<0.05)(表8和图1)。
表7 FFPW替代鱼粉对大口黑鲈幼鱼肠道消化酶活性的影响

Table 7 Effects of replacement of fish meal with FFPW on intestinal digestive enzyme activity of juvenile largemouth bass

项目
Items		 组别 Groups
FFPW0 FFPW10 FFPW20 FFPW40
脂肪酶 Lipase/(U/g) 15.87±1.59 16.36±2.02 16.75±1.54 16.28±1.99
α-淀粉酶 α-amylase/(U/mg) 0.34±0.04 0.33±0.04 0.35±0.05 0.38±0.04
胰蛋白酶 Trypsin/(U/mg) 186.32±16.67 180.61±15.41 185.56±18.42 192.29±22.16
表8 FFPW替代鱼粉对大口黑鲈幼鱼肠道组织结构的影响

Table 8 Effects of replacement of fish meal with FFPW on intestinal tissue structure of juvenile largemouth bassmm

项目
Items		 组别 Groups
FFPW0 FFPW10 FFPW20 FFPW40
绒毛长度 Villus length 0.70±0.14b 0.58±0.05a 0.61±0.07a 0.60±0.08a
绒毛宽度 Villus width 0.11±0.03 0.12±0.02 0.13±0.03 0.10±0.04
肌层厚度 Thickness of muscular layer 0.14±0.07a 0.17±0.02ab 0.13±0.03a 0.19±0.06b
图1 FFPW替代鱼粉对大口黑鲈幼鱼肠道组织的影响(HE染色)

VL:绒毛长度;VW:绒毛宽度;TML:肌层厚度。

Fig.1 Effects of FFPW on intestinal tissue structure of juvenile largemouth bass (HE staining)

VL: villus length; VW: villus width; TML: thickness of muscular layer.

3 讨论

3.1 FFPW替代鱼粉对大口黑鲈幼鱼生长和饲料效率的影响

水产加工副产物富含蛋白质、氨基酸、多不饱和脂肪酸、矿物质和生物活性物质等,是未来作为水产饲料蛋白质源的重要来源之一,通过生物技术的方法提高其利用率,将会产生明显的经济效益和生态效益[10]。采用微生物发酵或酶解技术来处理水产加工副产物/植物性蛋白质源,可改善其营养价值、降解抗营养因子、平衡氨基酸和提高适口性等,且酶菌协同效果更佳,适量的发酵产品添加到水产饲料中具有积极的效果[10,17⇓⇓-20]。本试验中,FFPW可替代大口黑鲈幼鱼饲料中10%~40%鱼粉而不会影响其成活率、生长性能和饲料利用率,这表明FFPW可替代10%~40%鱼粉作为大口黑鲈幼鱼饲料的蛋白质源。这可解释为采用植物乳杆菌固态发酵鲭鱼加工副产物与豆粕混合物,可将大分子蛋白质降解成易被鱼类消化吸收小肽和游离氨基酸等,充分降解大豆球蛋白和β-伴大豆球蛋白,产生的有机酸降低pH而且产品酱香浓郁,有助于提高饲料的适口性和蛋白质消化吸收[21]。Abdul Kader等[12]研究也发现,发酵豆粕与鱿鱼副产物(1∶1)替代12%~36%鱼粉对牙鲆(Paralichthys olivaceus)特定生长率无显著影响。类似地,以渔副产物和植物蛋白质混合发酵产物适量替代鱼粉对真鲷(Pagrus major)[11,13]、尖齿胡鲶(Clarias gariepinus)[22]、尼罗罗非鱼(Oreochromis niloticus)[23]和印度囊鳃鲶(Heteropneustes fossilis)[24]的生长和健康无显著影响。低鱼粉(30%)饲料中添加8%发酵鱼溶浆显著改善大菱鲆(Scophthalmus maximus)幼鱼对饲料蛋白质的利用率,并缓解高含量植物蛋白质引起的生长性能下降,且与高鱼粉组(50%)生长性能无显著差异[25]。在鱼粉含量为9%的基础饲料中,鲜杂鱼和豆粕(1∶1)混合发酵蛋白可替代奥尼罗非鱼稚鱼饲料中2/3鱼粉及鱼种饲料中100%鱼粉而不影响其生长,而100%替代引起罗非鱼稚鱼生长性能显著降低[26]。在真鲷[11,13]和牙鲆[12,17]的研究中发现,过量添加混合发酵豆粕与水产副产物导致生长和饲料利用率显著降低。这是因为水产加工副产品中骨骼比例大,其添加量过量引起饲料粗灰分含量过高,进而降低鱼类对饲料蛋白质和其他营养物质的消化利用率及生长[27-28],这可能是限制其在饲料中应用的主要因素。以上结果表明,水产饲料中添加水产加工副产物和植物蛋白质混合发酵产物是可行的,但适宜添加水平因鱼的种类和生长阶段、水产加工副产物和植物蛋白质源比例、发酵工艺和发酵产物添加量等的不同而存在差异。

3.2 FFPW替代鱼粉对大口黑鲈幼鱼体成分的影响

全鱼和肌肉成分是评价水产品质量的重要指标,其与饲料成分密切相关。本研究中,随着FFPW替代比例的升高,肌肉水分、全鱼水分和粗蛋白质含量呈降低的趋势,而肌肉和全鱼粗脂肪含量逐渐升高,这与研究者对印度囊鳃鲶[24]的研究结果一致,但与一些研究结果[11,25]相反。鱼体脂肪含量升高可能是由于饲料蛋氨酸含量不足减缓了肉碱的合成,进而抑制了脂肪酸β-氧化,而鱼体蛋白质含量降低可能是因为饲料蛋氨酸不足导致体蛋白质合成受阻[29]。还有研究发现,发酵豆粕与鱿鱼副产物替代鱼粉对牙鲆全鱼体成分无显著影响,而替代48%鱼粉导致鱼体蛋氨酸和苯丙氨酸含量及蛋白质沉积显著降低[12]。类似地,海产品副产物和大豆蛋白作为蛋白质源不会影响鱼体成分[13,17]。

3.3 FFPW替代鱼粉对大口黑鲈幼鱼血清生化指标及肝脏抗氧化指标的影响

血清生化指标是反映水产动物营养生理和健康状况的重要指标[30]。乳酸菌发酵鲭鱼糜对原发性高血压小鼠有显著的降胆固醇和降血糖作用[31]。高血脂大鼠灌喂2.5~10 mL/(kg·d)鳀鱼发酵制品均可显著降低其血清TC和TG含量和提高高密度脂蛋白胆固醇含量,这表明发酵水产品副产物能够促进高血脂大鼠的脂肪代谢,降低血脂含量[32]。本试验中,FFPW替代10%~40%鱼粉对血清AST、ALT和ALP活性以及TC和LDL含量无显著影响,这说明FFPW替代40%鱼粉对大口黑鲈肝脏功能无显著影响。随着FFPW替代比例的增加,血清TP含量逐渐升高,而血清GLU和TG含量逐渐降低,尤其是FFPW40组变化显著。血清TP含量升高,这说明适量添加FFPW有利于提高机体免疫力和代谢水平,促进蛋白质的吸收利用。发酵豆粕与鱿鱼副产物(1∶1)替代鱼粉对牙鲆血清GLU、TG含量和转氨酶活性无显著影响,但是提高血清TP含量和溶菌酶活性,减少致病菌数量[12]。在真鲷[11,13]、牙鲆[17]和大口黑鲈[18]的研究中也得到了类似的结果。不同研究者得出的血清生化指标数据存在差异可能与鱼类生理状态和对蛋白质源的吸收能力不同有关。
抗氧化防御系统对于清除机体过量积累的自由基和活性氧以保护机体免受氧化损伤至关重要[33]。SOD和CAT活性及T-AOC是动物机体健康和对应激反应的重要指标,较高的SOD、CAT活性和T-AOC说明细胞具有较高的清除自由基和分解过氧化物的能力[34-35]。本试验结果显示,FFPW替代10%~40%鱼粉对大口黑鲈肝脏SOD、CAT活性和T-AOC及MDA含量无显著影响,这表明FFPW替代鱼粉对大口黑鲈抗氧化能力无显著影响。类似地,未发酵或发酵金枪鱼副产物分别替代10%~50%、12.5%~50%鱼粉对牙鲆血清SOD和溶菌酶活性均无显著影响[17,36]。在大口黑鲈[18]、青鱼(Mylopharngodon piceus)[37]和大黄鱼(Pseudosciaena crocea)[38]的研究中,采用发酵豆粕替代鱼粉也得到了类似的结果。相反地,在大菱鲆[25]、珍珠龙胆石斑鱼(Epinephelus fuscoguttatus♀×E.lanceolatu )[39]和大口黑鲈[40]的研究中发现,饲料中添加水产加工副产物或发酵植物蛋白质源可提高鱼类抗氧化力和免疫力。这可解释为微生物发酵水产加工副产物等获得的多肽组分可以清除羟自由基、过氧化氢和超氧阴离子以及抑制DNA损伤,且分子质量越小的组分抗氧化活性越强[41-42]。此外,发酵过程中产生的酶类、有机酸、肽类等功能性因子可维持肠道微生态平衡、增强抗菌、抗病毒和免疫力[43-44]。

3.4 FFPW替代鱼粉对大口黑鲈幼鱼肠道消化酶活性和肠道组织结构的影响

鱼类的消化能力受消化酶活性的影响,并最终影响生长和健康[45]。本试验中,饲料中FFPW替代10%~40%鱼粉对肠道脂肪酶、α-淀粉酶和胰蛋白酶活性无显著影响,这是因为豆粕发酵可降解大部分抗营养因子,减轻豆粕对肠道的损伤,因而肠道消化酶活性未受到负面影响。研究者对罗非鱼[26]和青鱼[37]的研究也得到了类似结果。研究发现,随着海鲜副产品和大豆蛋白混合物添加水平的增加,粗蛋白质消化率呈下降趋势[13]。相反地,以5.4%虾水解物和11.2%发酵豆粕联合替代大口黑鲈饲料中鱼粉可显著提高蛋白质和氨基酸消化率[46]。胃蛋白酶活性随发酵蛋白替代量的增加而逐渐升高[23],这是因为蛋白质源经发酵产生的可溶性蛋白、寡糖和多肽可刺激酶的分泌,有助于提高蛋白质的消化和吸收[8-9,47]。此外,发酵产生的有机酸有利于促进酶活性[23]。
肠道结构的完整性是消化食物和吸收营养的前提条件及维持黏膜免疫功能的重要保障,其中肠道绒毛宽度、长度和肌层厚度是反映肠道结构和吸收能力的重要指标[48]。大豆等植物蛋白质中的抗营养因子在一定程度上会损伤鱼类肠道组织形态和肠黏膜屏障功能,引起肠炎病,从而降低消化酶活性和营养物质消化吸收率,最终会抑制鱼类的免疫力和生长[9,49-50]。目前,尚未见水产加工副产物和植物蛋白质混合发酵对水产动物肠道结构影响的相关报道。本研究表明,FFPW替代10%~40%鱼粉组肠道绒毛长度显著低于FFPW0组,但是肌层厚度高于FFPW0组,这说明FFPW和豆粕混合发酵对肠道结构具有一定的促进作用,有助于改善肠道功能,促进营养物质消化吸收,从而改善生产和健康状况。这与大多数有关发酵蛋白质源替代鱼粉对肠道结构的影响规律[51-52]一致。发酵蛋白质源对鱼类肠道结构的改善可能与发酵产生的酶类、有机酸、益生菌、小肽及黄酮类等活性物质有关[53]。

4 结论

本试验条件下,FFPW可替代大口黑鲈饲料中10%~40%鱼粉而不会影响其生长、饲料效率、肝脏抗氧化能力、肠道消化酶活性和肠道健康。

感谢日照职业技术学院海洋技术系张新明教授对文稿所提的宝贵意见。

References

Publishing order | Descend order by publishing year | Descend order by cited within
[1]
HUA K, COBCROFT J M, COLE A, et al. The future of aquatic protein:implications for protein sources in aquaculture diets[J]. One Earth, 2019, 1(3):316-329.

DOI

[2]
麦康森, 吕美东, 何艮. 水产饲料的蛋白源问题——提高饲料蛋白质利用率新思路[J]. 饲料工业, 2021, 42(1):2-6.

MAI K S, LV M D, HE G. The issue of protein sources of aquafeed-a new approach to improve utilization efficiency of feed protein[J]. Feed Industry, 2021, 42(1):2-6. (in Chinese)

[3]
申铉日, 李川, 夏光华. 水产品加工副产物的综合利用[M]. 北京: 科学出版社, 2018.

SHEN X R, LI C, XIA G H. Comprehensive utilization of aquatic product processing by-products[M]. Beijing: Science Press, 2018. (in Chinese)

[4]
GHALY A E, RAMAKRISHNAN V V, BROOKS M S, et al. Fish processing wastes as a potential source of proteins,amino acids and oils:a critical review[J]. Journal of Microbial & Biochemical Technology, 2013, 5(4):107-129.

[5]
SHAHIDI F, AMBIGAIPALAN P. Bioactives from seafood processing by-products[M]// MELTON L,SHAHIDI F,VARELIS P. Encyclopedia of Food Chemistry,Amsterdam:Elsevier, 2019:280-288.

[6]
SILA A, BOUGATEF A. Antioxidant peptides from marine by-products:isolation,identification and application in food systems. A review[J]. Journal of Functional Foods, 2016, 21:10-26.

DOI

[7]
TSAI T Y, HERNANDEZ L H H, GAYLORD T G, et al. Effects of dietary soybean meal inclusion on calcium-binding protein expression and inflammatory gene markers in liver and intestine of Atlantic Salmon (Salmo salar L.)[J]. Aquaculture Reports, 2023, 30:101624.

DOI

[8]
DAWOOD M A O, KOSHIO S. Application of fermentation strategy in aquafeed for sustainable aquaculture[J]. Reviews in Aquaculture, 2020, 12(2):987-1002.

DOI

[9]
MUGWANYA M, DAWOOD M A O, KIMERA F, et al. Replacement of fish meal with fermented plant proteins in the aquafeed industry:a systematic review and meta-analysis[J]. Reviews in Aquaculture, 2023, 15(1):62-88.

DOI

[10]
MARTI-QUIJAL F J, REMIZE F B E, MECA G, et al. Fermentation in fish and by-products processing:an overview of current research and future prospects[J]. Current Opinion in Food Science, 2020, 31:9-16.

DOI

[11]
ABDUL KADER M, KOSHIO S, ISHIKAWA M, et al. Growth,nutrient utilization,oxidative condition,and element composition of juvenile red Sea bream Pagrus major fed with fermented soybean meal and scallop by-product blend as fishmeal replacement[J]. Fisheries Science, 2011, 77(1):119-128.

DOI

[12]
ABDUL KADER M, KOSHIO S, ISHIKAWA M, et al. Can fermented soybean meal and squid by-product blend be used as fishmeal replacements for Japanese flounder (Paralichthys olivaceus)?[J]. Aquaculture Research, 2012, 43(10):1427-1438.

DOI

[13]
KADER M A, KOSHIO S. Effect of composite mixture of seafood by-products and soybean proteins in replacement of fishmeal on the performance of red Sea bream,Pagrus major[J]. Aquaculture, 2012, 368/369:95-102.

DOI

[14]
GUI J F, TANG Q S, LI Z J, et al. Aquaculture in China:success stories and modern trends[M]. Chichester: John Wiley & Sons Ltd, 2018:421-429.

[15]
农业农村部渔业渔政管理局,全国水产技术推广总站,中国水产学会. 2023中国渔业统计年鉴[M]. 北京: 中国农业出版社, 2023.

Fisheries and Fisheries Administration of the Ministry of Agriculture and Rural Affairs,National Aquatic Technology Promotion Station,China Society of Fisheries. 2023 China fishery statistical yearbook 2022[M]. Beijing: China Agriculture Press, 2023. (in Chinese)

[16]
XI L W, LU Q S, LIU Y L, et al. Effects of fish meal replacement with chlorella meal on growth performance,pigmentation,and liver health of largemouth bass (Micropterus salmoides)[J]. Animal Nutrition, 2022, 10:26-40.

DOI

[17]
ONCUL F O, AYA F A, SEONGHUN WON A H, et al. Effects of the dietary fermented tuna by-product meal on growth,blood parameters,nonspecific immune response,and disease resistance in juvenile olive flounder,Paralichthys olivaceus[J]. Journal of the World Aquaculture Society, 2019, 50(1):65-77.

DOI

[18]
陈晓瑛, 陈绍坚, 黄文, 等. 菌酶协同发酵豆粕替代鱼粉对大口黑鲈生长性能、血清生化、免疫和抗氧化指标及肝脏组织形态的影响[J]. 动物营养学报, 2021, 33(5):2848-2863.

DOI

CHEN X Y, CHEN S J, HUANG W, et al. Effects of fishmeal replacement by fermented soybean meal with bacteria and enzyme on growth performance, serum biochemical, immune and antioxidant indexes and hepatic histology of largemouth bass (Micropterus salmonides)[J]. Chinese Journal of Animal Nutrition, 2021, 33(5):2848-2863. (in Chinese)

[19]
FAGBENRO O A, BELLO-OLUSOJI O A. Preparation,nutrient composition and digestibility of fermented shrimp head silage[J]. Food Chemistry, 1997, 60(4):489-493.

DOI

[20]
王舒淇, 沙坤, 李雪, 等. 小黄鱼加工副产物发酵条件的优化及其营养评价[J]. 食品安全质量检测学报, 2021, 12(18):7160-7167.

WANG S Q, SHA K, LI X, et al. Optimization of fermentation conditions and nutritional evaluation of processing by-products of small yellow croaker[J]. Journal of Food Safety & Quality, 2021, 12(18):7160-7167. (in Chinese)

[21]
王瑶, 李红玉, 齐祥明, 等. 基于高通量测序的鲭鱼加工副产物固态厌氧发酵过程分析[J]. 南方水产科学, 2022, 18(4):136-146.

WANG Y, LI H Y, QI X M, et al. Analysis of solid-state anaerobic fermentation process of mackerel pro-cessing by-products by high-throughput sequencing[J]. South China Fisheries Science, 2022, 18(4):136-146. (in Chinese)

[22]
FAGBENRO O, JAUNCEY K. Growth and protein utilization by juvenile catfish (Clarias gariepinus) fed dry diets containing co-dried lactic-acid-fermented fish-silage and protein feedstuffs[J]. Bioresource Technology, 1995, 51(1):29-35.

DOI

[23]
FAGBENRO O A, JAUNCEY K. Physical and nutritional properties of moist fermented fish silage pellets as a protein supplement for tilapia (Oreochromis niloticus)[J]. Animal Feed Science and Technology, 1998, 71(1/2):11-18.

DOI

[24]
MONDAL K, KAVIRAJ A, MUKHOPADHYAY P K. Evaluation of fermented fish-offal in the formulated diet of the freshwater catfish Heteropneustes fossilis[J]. Aquaculture Research, 2008, 39(13):1443-1449.

DOI

[25]
许聪, 王际英, 郝甜甜, 等. 发酵鱼溶浆替代鱼粉对大菱鲆幼鱼生长、抗氧化能力、蛋白质代谢及相关基因表达的影响[J]. 渔业科学进展, 2023, 44(1):90-102.

XU C, WANG J Y, HAO T T, et al. The effect of replacing fish meal with fermented stickwater on growth,antioxidant capacity,protein metabolism and related gene expression of juvenile turbot(Scophthalmus maximus L.)[J]. Progress in Fishery Sciences, 2023, 44(1):90-102. (in Chinese)

[26]
刘勇, 冷向军, 李小勤, 等. 混合发酵蛋白替代鱼粉对奥尼罗非鱼幼鱼生长、营养物质消化率及血清非特异性免疫的影响[J]. 上海海洋大学学报, 2009, 18(2):160-166.

LIU Y, LENG X J, LI X Q, et al. Effect of fermented mixure-protein replacing fish meal on growth,apparent digestibility coefficients and serum non-specific immunity of tilapia(Oreochromis niloticus×O.aureus)[J]. Journal of Shanghai University, 2009, 18(2):160-166. (in Chinese)

[27]
GODDARD S, AL-SHAGAA G, ALI A. Fisheries by-catch and processing waste meals as ingredients in diets for Nile tilapia,Oreochromis niloticus[J]. Aquaculture Research, 2008, 39(5):518-525.

DOI

[28]
NAYLOR R L, HARDY R W, BUREAU D P, et al. Feeding aquaculture in an era of finite resources[J]. PNAS, 2009, 106(36):15103-15110.

DOI PMID

[29]
LANGAR H, GUILLAUME J, METAILLER R, et al. Augmentation of protein synthesis and degradation by poor dietary amino acid balance in European sea bass (Dicentrarchus labrax)[J]. The Journal of Nutrition, 1993, 123(10):1754-1761.

DOI

[30]
EL-OUNY Y M, MAULU S, ZAKI M A A, et al. Effect of fishmeal replacement with dried red wigglers (Eisenia fetida) worm meal on growth and feed utilization,production efficiency, and serum biochemistry in Nile tilapia (Oreochromis niloticus) fingerlings[J]. Aquaculture Reports, 2023, 29:101518.

DOI

[31]
YIN L J, TONG Y L, JIANG S T. Improvement of the functionality of minced mackerel by hydrolysis and subsequent lactic acid bacterial fermentation[J]. Journal of Food Science, 2005, 70(3):M172-M178.

DOI

[32]
洪詠平, 张虹, 张政委, 等. 鳀鱼发酵制品对高血脂大鼠血脂水平的影响[J]. 中国食品学报, 2005, 5(2):94-97.

HONG Y P, ZHANG H, ZHANG Z W, et al. Effects of silver anchovy-fermentation product on plasma lipid level in the rats with hyperlipaemia[J]. Journal of Chinese Institute of Food Science and Technology, 2005, 5(2):94-97. (in Chinese)

[33]
PETITJEAN Q, JEAN S, GANDAR A, et al. Stress responses in fish:from molecular to evolutionary processes[J]. Science of the Total Environment, 2019, 684:371-380.

DOI

[34]
WOJTCZYK-MIASKOWSKA A, SCHLICHTHOLZ B. DNA damage and oxidative stress in long-lived aquatic organisms[J]. DNA Repair, 2018, 69:14-23.

DOI

[35]
LIM S J, LEE K J. A microbial fermentation of soybean and cottonseed meal increases antioxidant activity and gossypol detoxification in diets for Nile tilapia,Oreochromis niloticus[J]. Journal of the World Aquaculture Society, 2011, 42(4):494-503.

DOI

[36]
KIM J, BAEK S I, CHO S H, et al. Evaluating the efficacy of partially substituting fish meal with unfermented tuna by-product meal in diets on the growth,feed utilization,chemical composition and non-specific immune responses of olive flounder (Paralichthys olivaceus)[J]. Aquaculture Reports, 2022, 24:101150.

DOI

[37]
陈倪慧, 杨霞, 孙珊珊, 等. 发酵植物蛋白复配替代豆粕对青鱼生长、免疫、抗氧化及肠道菌群结构的影响[J]. 动物营养学报, 2023, 35(4):2478-2489.

DOI

CHEN N H, YANG X, SUN S S, et al. Effects of soybean meal replaced by fermented plant protein compound on growth,immune,antioxidant and intestinal microflora structure of black carp(Mylopharyngodon piceus)[J]. Chinese Journal of Animal Nutrition, 2023, 35(4):2478-2489. (in Chinese)

[38]
李春梅, 林娟. 豆粕发酵工艺优化及发酵豆粕替代部分鱼粉对大黄鱼的饲喂效果[J]. 动物营养学报, 2022, 34(1):563-574.

DOI

LI C M, LIN J. Optimization of soybean meal fermentation process and feeding effect of dietary fish meal partial replacement by fermented soybean meal for large yellow croaker[J]. Chinese Journal of Animal Nutrition, 2022, 34(1):563-574. (in Chinese)

[39]
王晓艳, 马季, 王际英, 等. 鱼溶浆粉在珍珠龙胆石斑鱼幼鱼的高植物蛋白饲料中的应用[J]. 中国海洋大学学报(自然科学版), 2021, 51(1):31-43.

WANG X Y, MA J, WANG J Y, et al. Studies on supplementation of stickwater meal to high plant protein diets of juvenile Epinephelus fuscoguttatus ♀×E.lanceolatus ♂ pearl gentian[J]. Periodical of Ocean University of China, 2021, 51(1):31-43. (in Chinese)

[40]
黄河, 田鑫鑫, 黄旭雄, 等. 发酵豆粕替代鱼粉对大口黑鲈幼鱼生长、脂质代谢、血清非特异性免疫及肠道菌群的影响[J]. 水生生物学报, 2022, 46(4):466-477.

HUANG H, TIAN X X, HUANG X X, et al. Fermented soybean meal instead of fish meal on growth,lipid metabolism,serum non-specific immunity and intestinal flora of juvenile largemouth bass[J]. Acta Hydrobiologica Sinica, 2022, 46(4):466-477. (in Chinese)

[41]
贾晨, 李静媛, 金玉兰, 等. 章鱼下脚料发酵液中多肽的分离及抗氧化活性的研究[J]. 青岛农业大学学报(自然科学版), 2015, 32(1):36-41.

JIA C, LI J Y, JIN Y L, et al. Antioxidative bioactivity of polypeptide derived from octopus waste broth[J]. Journal of Qingdao Agricultural University(Natural Science), 2015, 32(1):36-41. (in Chinese)

[42]
张京楼. 鳕鱼皮多肽的益生菌发酵工艺探索及体外抗氧化性能研究[D]. 硕士学位论文. 烟台: 烟台大学, 2012.

ZHANG J L. Preparation of peptides by probiotic fermentation from cod skin and its antioxidant properties in vitro[D]. Master’s Thesis. Yantai: Yantai University, 2012. (in Chinese)

[43]
NAJAFIAN L, BABJI A S. Fractionation and identification of novel antioxidant peptides from fermented fish (pekasam)[J]. Journal of Food Measurement and Characterization, 2018, 12(3):2174-2183.

DOI

[44]
ADESULU-DAHUNSI A T, DAHUNSI S O, OLAYANJU A. Synergistic microbial interactions between lactic acid bacteria and yeasts during production of Nigerian indigenous fermented foods and beverages[J]. Food Control, 2020, 110:106963.

DOI

[45]
SHAN X J, XIAO Z Z, HUANG W, et al. Effects of photoperiod on growth,mortality and digestive enzymes in miiuy croaker larvae and juveniles[J]. Aquaculture, 2008, 281(1/2/3/4):70-76.

DOI

[46]
LI S L, DAI M, QIU H J, et al. Effects of fishmeal replacement with composite mixture of shrimp hydrolysate and plant proteins on growth performance,feed utilization,and target of rapamycin pathway in largemouth bass, Micropterus salmoides[J]. Aquaculture, 2021, 533:736185.

DOI

[47]
HARNEDY P A, FITZGERALD R J. Bioactive peptides from marine processing waste and shellfish:a review[J]. Journal of Functional Foods, 2012, 4(1):6-24.

DOI

[48]
张卫, 谭北平, 庞奥博, 等. 珍珠龙胆石斑鱼豆粕诱导型肠炎肠道潜在生物标志物筛选[J]. 广东海洋大学学报, 2022, 42(4):1-12.

ZHANG W, TAN B P, PANG A B, et al. Screening of potential biomarkers for soybean meal induced enteritis in pearl gentian grouper (Epinephelus fuscoguttatus♀×Epinephelus lanceolatus ♂)[J]. Journal of Guangdong Ocean University, 2022, 42(4):1-12. (in Chinese)

[49]
FRANCIS G, MAKKAR H P S, BECKER K. Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish[J]. Aquaculture, 2001, 199(3/4):197-227.

DOI

[50]
KROGDAHL Å, BAKKE-MCKELLEP A M, BAEVERFJORD G. Effects of graded levels of standard soybean meal on intestinal structure,mucosal enzyme activities,and pancreatic response in Atlantic salmon (Salmo salar L.)[J]. Aquaculture Nutrition, 2003, 9(6):361-371.

DOI

[51]
REFSTIE S, SAHLSTRÖM S, BRÅTHEN E, et al. Lactic acid fermentation eliminates indigestible carbohydrates and antinutritional factors in soybean meal for Atlantic salmon (Salmo salar)[J]. Aquaculture, 2005, 246(1/2/3/4):331-345.

DOI

[52]
钟国防, 田鑫鑫, 谢春元, 等. 芽孢杆菌有氧发酵豆粕替代鱼粉对大口黑鲈幼鱼生长性能、血清生化指标及肠组织结构的影响[J]. 渔业科学进展, 2021, 42(5):139-148.

ZHONG G F, TIAN X X, XIE C Y, et al. Effects of replacing fish meal with bacillus aerobically fermented soybean meal on the growth performance,serum biochemical indices and intestinal histology of largemouth bass (Micropterus salmoides)[J]. Progress in Fishery Sciences, 2021, 42(5):139-148. (in Chinese)

[53]
卞宇豪, 杨航, 许晓莹, 等. 发酵豆粕、肉骨粉及其混合物替代鱼粉对大口黑鲈生长、血清生化指标和肠道组织学的影响[J]. 水产学报, 2022, 46(10):1813-1823.

BIAN Y H, YANG H, XU X Y, et al. Effects of replacing dietary fish meal with fermented soybean meal,meat and bone meal and their mixture on growth,serum biochemical indices and intestinal histology of largemouth bass (Micropterussalmoides)[J]. Journal of Fisheries of China, 2022, 46(10):1813-1823. (in Chinese)

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