Chinese Journal of Animal Nutrition >

2026 , Vol. 38 >Issue 5: 3592 - 3607

DOI: https://doi.org/10.12418/CJAN2026.287

RESEARCH PAPER

Effects of Different Protein Sources Replacing Fish Meal on Growth Performance, Serum Biochemical Indices, Liver and Intestinal Health of Bullfrog (Aquarana catesbeiana)

  • WANG Menghua , 1, 2 ,
  • YE Weibin 1 ,
  • HUANG Wenqing 2 ,
  • WANG Suitao 2 ,
  • WEI Zhenhai 2 ,
  • ZHOU Meng 1 ,
  • HUANG Yanhua , 1, *
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  • 1 Innovative Institute of Animal Healthy Breeding, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, China
  • 2 Guangzhou Fishtech Fisheries Science and Technology Co., Ltd., Guangzhou 510640, China
*professor, E-mail:

Received date: 2025-10-11

  Online published: 2026-05-14

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Abstract

This experiment was conducted to investigate the effects of different protein sources replacing fish meal on growth performance, serum biochemical indices, liver and intestinal health of bullfrog (Aquarana catesbeiana). A basal diet with 8% fish meal was formulated as the control group (CK group), and 37.5% of the fish meal in the basal diet was replaced with dried Hermetia illucens L. larvae (B group), defatted dried Hermetia illucens L. larvae (D group), rapeseed meal (R group) or cottonseed meal (C group), respectively. Five isonitrogenous and isolipidic experimental diets were prepared. A total of 1 200 healthy bullfrog (Aquarana catesbeiana) with an initial body weight of approximately 40 g were randomly divided into 5 groups, each with 3 replicates of 80 bullfrog, and fed the corresponding diets for 56 days. The results showed as follows: 1) the final body weight, weight gain rate and specific growth rate in B group and D group were not significantly different from those in CK group (P>0.05), whereas these indices in R group and C group were significantly lower than those in CK group (P<0.05). The feed conversion ratio in B group and D group showed no significant difference compared with CK group (P>0.05), while it was significantly higher in R group and C group than in CK group (P<0.05). 2) The redness (a*) and yellowness (b*) values of hind leg muscle in B group and D group were not significantly different from those in CK group (P>0.05), but were significantly lower than those in R group and C group (P<0.05). 3) The contents of serum albumin (ALB), low-density lipoprotein cholesterol (LDL-C), cholesterol (CHO), high-density lipoprotein cholesterol (HDL-C), as well as the activities of aspartate aminotransferase (AST) and alanine aminotransferase (ALT) in B group and D group exhibited no significant differences compared with CK group (P>0.05). However, the serum ALB and LDL-C contents as well as AST and ALT activities in B group and D group were significantly lower than those in R group and C group (P<0.05), while the serum CHO and HDL-C contents were significantly higher than those in R group and C group (P<0.05). 4) The activities of superoxide dismutase (SOD) and catalase (CAT), total antioxidant capacity (T-AOC) and malondialdehyde (MDA) content in liver of B group and D group were not significantly different from those in CK group (P>0.05). Nevertheless, the SOD and CAT activities and T-AOC in liver of B group and D group were significantly higher than those in R group and C group (P<0.05), and the MDA content was significantly lower than that in R group and C group (P<0.05). 5) The intestinal wall thickness in B group and D group was not significantly different from that in CK group (P>0.05), but was significantly higher than that in R group and C group (P<0.05). Autolysis of intestinal epithelial cells and irregular arrangement of columnar epithelial cells were observed in C group. In conclusion, replacing 37.5% of fish meal with dried Hermetia illucens L. larvae and defatted dried Hermetia illucens L. larvae in the diet has no adverse effects on the growth performance, serum biochemical indices, antioxidant capacity and intestinal morphology of bullfrog (Aquarana catesbeiana), and exerts a certain protective effect on liver health.

Key words： bullfrog (Aquarana catesbeiana); Hermetia illucens L.; plant protein source; fish meal; growth performance; liver health

Cite this article

WANG Menghua , YE Weibin , HUANG Wenqing , WANG Suitao , WEI Zhenhai , ZHOU Meng , HUANG Yanhua . Effects of Different Protein Sources Replacing Fish Meal on Growth Performance, Serum Biochemical Indices, Liver and Intestinal Health of Bullfrog (Aquarana catesbeiana)[J]. Chinese Journal of Animal Nutrition, 2026 , 38(5) : 3592 -3607 . DOI: 10.12418/CJAN2026.287

鱼粉具有营养均衡、适口性好和抗营养因子含量低的优点,作为优质蛋白质源在水产饲料中发挥着重要作用[1]。随着水产养殖业的发展,鱼粉需求量持续增长,但受限于海洋资源与环保要求,鱼粉供应日益紧张[2]。为促进水产养殖业的可持续发展,寻找可替代鱼粉的蛋白质源已成为国内外水产饲料领域的重要研究方向。目前,植物蛋白质源与昆虫蛋白质源等替代原料已引起广泛关注。黑水虻幼虫粉的营养成分与鱼粉接近[3],且虫体含有抗菌肽[4]、月桂酸[5]、壳聚糖[6]等活性成分。研究表明,适量使用黑水虻幼虫粉替代鱼粉,对欧洲黑鲈(Dicentrarchus labrax)[7]、黄颡鱼(Pelteobagrus fulvidraco)[8]、凡纳滨对虾(Litopenaeus vannamei)[9]的健康具有积极影响;使用脱脂黑水虻虫粉替代饲料中不超过40%的鱼粉,可促进大黄鱼(Larimichthys crocea)的生长及肠道健康[10];使用黑水虻幼虫粉替代尼罗罗非鱼(Oreochromis niloticus)饲料中10%~100%的鱼粉,对其生长性能无负面影响[11]。植物蛋白质源价格低廉、数量丰富、供应稳定,已被广泛应用于水产养殖中[12]。菜籽粕是油菜籽榨油后的副产物,油菜籽为我国第2大油料作物,资源储备丰富[13]。菜籽粕的粗蛋白质、钙和磷含量均低于鱼粉,同时含有硫代葡萄糖苷等抗营养因子,限制了其在水产饲料中的规模化应用[14]。研究发现,菜籽粕替代饲料中30%的鱼粉时,不会影响虹鳟鱼(Oncorhynchus mykiss)的生长性能,但若替代比例超过50%,则会导致其生长性能显著降低[15];当菜籽粕替代鱼粉的比例不超过20%时,对异育银鲫(Carassius auratus gibelio)的生长和饲料转化效率无不良影响[16]。棉籽粕是水产饲料中常见的植物蛋白质源[17],但其含有棉酚等抗营养因子,且氨基酸含量不平衡,一定程度上限制了其在水产养殖上的应用[18]。研究发现,棉籽粕替代凡纳滨对虾饲料中不超过40%的鱼粉,对其生长、饲料利用率和存活率无显著影响[19];当饲料中棉籽粕添加比例超过15%时,虹鳟鱼幼鱼的增重率显著降低[20]。牛蛙(Aquarana catesbeiana)作为我国极具发展潜力的养殖品种,具有易养殖、生长繁殖速度快、环境适应能力强、食性杂、饵料利用率高等优点[21-22]。其肉质洁白细嫩、营养丰富,属于高蛋白质、低脂肪、低胆固醇的健康食品,且蛙皮和蛙油还在医药、化工领域具有重要应用价值[23]。为推动牛蛙养殖业的可持续发展,开发新型蛋白质源及低鱼粉饲料势在必行。因此,本试验采用菜籽粕、棉籽粕及不同脂肪含量的黑水虻干虫替代饲料中37.5%的鱼粉,探究其对牛蛙生长性能、血清生化指标及肝脏和肠道健康的影响,旨在验证上述蛋白质源替代鱼粉在牛蛙饲料中应用的可行性,为降低牛蛙饲料中鱼粉的用量提供理论依据。

1 材料与方法

1.1 试验饲料

以豆粕、鱼粉、猪肉粉和鸡肉粉等为主要蛋白质源,大豆油和鱼油为主要脂肪源,高筋面粉为主要碳水化合物源,配制含8%鱼粉的基础饲料(CK组,作为对照组),然后在基础饲料配方的基础上,分别以黑水虻干虫(B组)、脱脂黑水虻干虫(D组)、菜籽粕(R组)和棉籽粕(C组)替代37.5%的鱼粉,共制成5种等氮等脂的试验饲料。原料的粉碎与混合步骤参照王梦华等[24],将混合均匀的原料经TSE-65S型膨化机(北京现代洋工机械科技发展有限公司)加工为粒径1.5 cm的膨化饲料,于55 ℃烘2 h,自然冷却后将油脂与饲料充分混匀,置于8 ℃恒温饲料房保存备用。黑水虻干虫与脱脂黑水虻干虫的营养成分见表1,试验饲料组成及营养水平见表2。
表1 黑水虻干虫与脱脂黑水虻干虫的营养成分(风干基础)

Table 1 Nutritional components of dried Hermetia illucens L. larvae and defatted dried Hermetia illucens L. larvae (air-dry basis)%

项目
Items		 黑水虻干虫
Dried Hermetia illucens L. larvae		 脱脂黑水虻干虫
Defatted dried Hermetia illucens L. larvae
粗蛋白质 CP 40.38 55.50
粗脂肪 EE 30.55 10.32
水分 Moisture 6.12 5.83
粗灰分 Ash 9.60 10.58
钙 Ca 2.61 2.90
磷 P 0.58 0.62
酸溶蛋白 Acid-soluble protein 5.02 6.82
天门冬氨酸 Asp 2.36 3.18
谷氨酸 Glu 4.41 6.20
丝氨酸 Ser 1.27 1.68
组氨酸 His 0.61 0.86
甘氨酸 Gly 1.47 2.13
苏氨酸 Thr 1.19 1.70
精氨酸 Arg 1.93 2.62
丙氨酸 Ala 2.43 3.30
酪氨酸 Tyr 1.22 1.62
缬氨酸 Val 2.00 2.63
蛋氨酸 Met 0.43 0.62
苯丙氨酸 Phe 0.99 1.33
异亮氨酸 Ile 1.29 1.74
亮氨酸 Leu 1.93 2.60
赖氨酸 Lys 1.57 2.20
多肽 Polypeptide 25.08 34.25
壳聚糖 Chitosan 0.48 0.62
胆固醇 CHO 1.75 2.34
月桂酸 Lauric acid 4.59 1.60
表2 试验饲料组成及营养水平(风干基础)

Table 2 Composition and nutrient levels of experimental diets (air-dry basis)%

项目
Items		 组别 Groups
CK B D R C
原料 Ingredients
鱼粉 Fish meal 8.00 5.00 5.00 5.00 5.00
鸡肉粉 Chicken powder 6.00 6.00 6.00 6.00 6.00
猪肉粉 Pork powder 14.00 14.00 14.00 14.00 14.00
血球蛋白粉 Hemoglobin powder 4.00 4.00 4.00 4.00 4.00
豆粕 Soybean meal 30.00 30.00 30.00 30.00 30.00
大豆浓缩蛋白 Soy protein concentrate 2.00 2.00 2.00 2.00 2.00
高筋面粉 Bread flour 25.00 25.00 25.00 25.00 25.00
黑水虻干虫 Dried Hermetia illucens L. larvae 4.54
脱脂黑水虻干虫 Defatted dried Hermetia illucens L. larvae 3.93
菜籽粕 Rapeseed meal 3.98
棉籽粕 Cottonseed meal 3.23
鱼油 Fish oil 1.00 1.00 1.00 1.00 1.00
大豆油 Soybean oil 2.50 1.00 1.82 2.67 2.74
微晶纤维素 Microcrystalline cellulose 4.70 4.66 4.45 3.55 4.23
维生素预混料 Vitamin premix1) 0.50 0.50 0.50 0.50 0.50
矿物质预混料 Mineral premix2) 0.10 0.10 0.10 0.10 0.10
磷酸二氢钙 Ca(H2PO4)2 1.50 1.50 1.50 1.50 1.50
维生素C磷酸酯 Vitamin C phosphate ester 0.20 0.20 0.20 0.20 0.20
蛋氨酸 Met3) 0.50 0.50 0.50 0.50 0.50
合计 Total 100.00 100.00 100.00 100.00 100.00
营养水平 Nutrient levels4)
粗蛋白质 CP 38.32 38.25 38.21 38.34 38.58
粗脂肪 EE 6.20 6.19 6.19 6.20 6.20
水分 Moisture 6.03 6.12 6.11 6.06 6.11
粗灰分 Ash 10.60 10.88 10.69 10.65 10.65

1)每千克维生素预混料含有 One kilogram of vitamin premix contained the following:VA 4 000 000 IU,VD3 2 000 000 IU,VE 30 g,VK3 10 g,VB1 5 g,VB2 15 g,VB6 8 g,泛酸钙 calcium pantothenate 25 g,叶酸folic acid 2.5 g,生物素 biotin 0.08 g,烟酸 nicotinic acid 40 g,VB12 0.02 g,肌醇 inositol 150 g。

2)每千克矿物质预混料含有 One kilogram of mineral premix contained the following:MgSO4·H2O 12 g,KCl 90 g,Met-Cu 3 g,FeSO4·H2O 1 g,ZnSO4·H2O 10 g,Ca (IO3)2 0.06 g,Met-Co 0.16 g,Na2SeO3 0.003 6 g。

3)50%包膜结构的蛋氨酸。50% encapsulated methionine.

4)营养水平为实测值。Nutrient levels were measured values.

1.2 试验动物与饲养管理

牛蛙由惠州市财兴实业有限公司牛蛙养殖基地提供,并在该基地进行养殖试验。动物试验程序经仲恺农业工程学院实验动物伦理委员会批准,批准号为ZK20252202。选取初始体重约40 g的健康牛蛙1 200只,随机分为5组,每组3个重复,将实际生产中所用养殖土池改造为试验网箱(规格1 m×0.5 m×0.6 m),采用高密度养殖模式,每个网箱(重复)放养80只牛蛙,分别饲喂相应的试验饲料,进行为期56 d的养殖试验。采用表观饱食投喂方式,每天于08:00和17:00各投喂1次。养殖用水为经2 d曝晒与曝气处理的地下水,试验期间每5~7 d进行1次全池换水;养殖期间水温维持在25~31 ℃,氨氮浓度<0.20 mg/L,亚硝酸盐浓度<0.1 mg/L,pH为7.30~8.20。养殖过程中每天记录各重复的饲料消耗量与牛蛙死亡情况。

1.3 样品采集

养殖试验结束后停食1 d,统计存活率,并称量每只牛蛙终末体重。从每个重复中随机选取8只牛蛙,其中3只使用1 mL无菌注射器进行心脏采血,血液在4 ℃环境静置4 h后,4 ℃下以2 200×g离心10 min,将上清液分装置于-80 ℃保存,以检测血清生化指标。剩余5只牛蛙去除头、爪、皮后称重,计算净肉率;称量内脏团重量,计算脏体比;剪取左后腿称重,计算后腿肉率,随后剥离腿部肌肉,测定pH与肉色;取出肝脏并称重,计算肝体比,然后将每块肝脏均分为2份,一份置于-80 ℃低温保存,用于测定抗氧化指标,另一份放入4%多聚甲醛溶液中固定,用于肝脏形态结构检测;取中肠组织,放入4%多聚甲醛溶液中固定保存,用于肠道形态结构检测。

1.4 指标测定

1.4.1 饲料及原料常规营养成分

粗脂肪含量采用GB/T 6433—2025的方法测定,粗灰分含量采用GB/T 6438—2007的方法测定,水分含量采用GB/T 6435—2014的方法测定,粗蛋白质含量采用GB/T 6432—2018的方法测定,钙含量采用GB/T 6436—2018的方法测定,磷含量采用GB/T 6437—2018的方法测定,酸溶蛋白含量采用NY/T 3801—2020的方法测定,胆固醇(CHO)含量采用GB 5009.128—2016的方法测定,多肽、氨基酸和月桂酸含量采用高效液相色谱法测定。壳聚糖以盐酸氨基葡萄糖计,样品经酸水解后采用高效液相色谱法测定。

1.4.2 生长性能和屠宰性能

相关指标计算公式如下:

增重率(WGR,%)=100×(终末体重-

初始体重)/初始体重;

存活率(SR,%)=100×终末数量/初始数量;

特定生长率(SGR,%/d)=100×(ln终末体重-

ln初始体重)/养殖天数;

饲料系数(FCR)=总耗料量/(终末体重+

死亡体重-初始体重);

肝体比(HSI,%)=100×肝脏重/体重;

脏体比(VSI,%)=100×内脏重/体重;

净肉率(%)=100×净肉重/体重;

后腿肉率(%)=100×左后腿去皮重×2/体重。

1.4.3 后腿肌肉pH及肉色

参照Petracci等[25]的方法测定后腿肌肉pH及肉色[亮度(L*)、红度(a*)和黄度(b*)值]。

1.4.4 血清生化指标

委托广州新海医院检测科对血清葡萄糖(GLU)、CHO、甘油三酯(TG)、低密度脂蛋白胆固醇(LDL-C)、高密度脂蛋白胆固醇(HDL-C)、总蛋白(TP)、白蛋白(ALB)含量及谷草转氨酶(AST)、碱性磷酸酶(ALP)、谷丙转氨酶(ALT)、乳酸脱氢酶(LDH)活性进行检测。

1.4.5 肝脏抗氧化指标

采用南京建成生物工程研究所生产的试剂盒测定肝脏丙二醛(MDA)含量、总抗氧化能力(T-AOC)及过氧化氢酶(CAT)、超氧化物歧化酶(SOD)活性,具体操作步骤参照试剂盒说明书执行。

1.4.6 肝脏和肠道形态结构

肝脏和肠道组织石蜡切片的制作与观察步骤如下:将组织样品从4%多聚甲醛溶液中取出,用手术刀取相同部位组织,经不同浓度乙醇梯度脱水,二甲苯透明后石蜡包埋,制作5 μm厚的切片。采用常规组织学方法进行油红O染色与苏木精-伊红(HE)染色。利用光学显微镜(DP72,Olympus,日本)观察染色结果,并将显微镜连接至装有Motic Images软件(Leica Application Suite v3.3.0)的计算机进行图像采集与分析。

1.5 数据统计分析

利用SPSS 26.0软件对试验数据进行单因素方差分析(one-way ANOVA),并采用Duncan氏法进行组间多重比较。结果用平均值±标准误(mean±SE)表示,以P<0.05为差异显著。

2 结果与分析

2.1 不同蛋白质源替代鱼粉对牛蛙生长性能的影响

由表3可知,各组间初始体重和存活率无显著差异(P>0.05)。与CK组相比,各替代组终末体重、增重率和特定生长率均有所降低,其中B组和D组与CK组无显著差异(P>0.05),R组和C组则显著低于CK组(P<0.05),且R组显著低于其他各组(P<0.05)。CK组饲料系数与B组和D组无显著差异(P>0.05),而显著低于C组(P<0.05),且C组饲料系数显著低于R组(P<0.05)。
表3 不同蛋白质源替代鱼粉对牛蛙生长性能的影响

Table 3 Effects of different protein sources replacing fish meal on growth performance of bullfrog (Aquarana catesbeiana)

项目
Items		 组别 Groups
CK B D R C
初始体重 IBW/g 41.88±0.62 42.08±0.36 42.08±0.36 42.29±0.36 42.08±0.95
终末体重 FBW/g 164.01±1.72c 163.03±1.12c 162.59±2.37c 142.18±5.98a 156.30±1.22b
增重率 WGR/% 291.68±3.05c 287.41±1.86c 286.39±8.60c 236.13±11.42a 271.54±9.72b
特定生长率 SGR/(%/d) 2.44±0.01c 2.42±0.01c 2.41±0.04bc 2.16±0.06a 2.34±0.05b
存活率 SR/% 99.58±0.72 99.17±1.44 99.17±1.44 98.75±1.25 99.17±0.72
饲料系数 FCR 1.02±0.01a 1.04±0.01ab 1.08±0.03ab 1.26±0.07c 1.10±0.02b

同行数据肩标无字母或相同小写字母表示差异不显著(P>0.05),不同小写字母表示差异显著(P<0.05)。下表同。

In the same row, values with no letter or the same small letter superscripts mean no significant difference (P>0.05), while with different small letter superscripts mean significant difference (P<0.05). The same as below.

2.2 不同蛋白质源替代鱼粉对牛蛙屠宰性能的影响

由表4可知,各组牛蛙的肝体比、脏体比、净肉率和后腿肉率均无显著差异(P>0.05)。
表4 不同蛋白质源替代鱼粉对牛蛙屠宰性能的影响

Table 4 Effects of different protein sources replacing fish meal on slaughter performance of bullfrog (Aquarana catesbeiana)%

项目
Items		 组别 Groups
CK B D R C
肝体比 HSI 3.57±0.54 3.49±0.39 3.22±0.69 3.71±1.46 3.63±0.92
脏体比 VSI 16.71±1.09 16.50±1.37 16.75±1.34 17.27±1.95 16.53±1.04
净肉率 Dressed meat percentage 52.20±2.42 54.18±2.10 52.34±2.81 53.08±6.18 53.24±3.28
后腿肉率 Hind leg meat percentage 26.50±2.74 25.86±2.79 25.47±1.39 26.35±2.98 27.02±2.50

2.3 不同蛋白质源替代鱼粉对牛蛙后腿肌肉品质的影响

由表5可知,各组间后腿肌肉pH和L*值无显著差异(P>0.05)。B组和D组后腿肌肉a*和b*值与CK组无显著差异(P>0.05),但显著低于R组和C组(P<0.05)。
表5 不同蛋白质源替代鱼粉对牛蛙后腿肌肉品质的影响

Table 5 Effects of different protein sources replacing fish meal on hind leg muscle quality of bullfrog (Aquarana catesbeiana)

项目
Items		 组别 Groups
CK B D R C
pH 7.19±0.04 7.18±0.12 7.10±0.03 7.09±0.14 7.13±0.02
亮度 L* 57.94±1.08 57.58±0.71 57.90±0.37 57.19±0.11 57.17±0.28
红度 a* 6.37±0.02a 6.38±0.04a 6.59±0.13a 7.31±0.22b 7.33±0.06b
黄度 b* 6.21±0.06a 6.25±0.08a 6.24±0.12a 6.63±0.08b 6.64±0.05b

2.4 不同蛋白质源替代鱼粉对牛蛙血清生化指标的影响

由表6可知,B组和D组血清ALB、LDL-C含量及AST、ALT活性与CK组无显著差异(P>0.05),但显著低于R组和C组(P<0.05);各替代组血清TG含量与CK组无显著差异(P>0.05),但较CK组有所降低;R组血清球蛋白(GLOB)含量显著低于CK组和B组(P<0.05);各组血清LDH含量差异显著(P<0.05),由低到高依次为B组<CK组<D组<C组<R组;B组和D组血清CHO和HDL-C含量与CK组无显著差异(P>0.05),但显著高于R组和C组(P<0.05);CK组、B组和D组血清ALP活性和GLU含量显著低于R组和C组(P<0.05)。
表6 不同蛋白质源替代鱼粉对牛蛙血清生化指标的影响

Table 6 Effects of different protein sources replacing fish meal on serum biochemical indices of bullfrog (Aquarana catesbeiana)

项目
Items		 组别 Groups
CK B D R C
胆固醇 CHO/(mmol/L) 0.48±0.01b 0.48±0.01b 0.48±0.01b 0.46±0.01a 0.46±0.01a
甘油三酯 TG/(mmol/L) 0.35±0.01 0.33±0.01 0.34±0.01 0.34±0.02 0.34±0.01
谷丙转氨酶 ALT/(U/L) 12.51±0.06ab 12.39±0.04a 12.57±0.02b 13.60±0.05d 13.12±0.12c
谷草转氨酶 AST/(U/L) 75.97±0.46a 76.11±0.81a 76.26±0.53a 82.84±0.25c 81.35±0.49b
总蛋白 TP/(g/L) 32.58±0.31 32.89±0.44 32.49±0.24 32.89±0.50 32.64±0.55
白蛋白 ALB/(g/L) 18.32±0.11a 18.39±0.08a 18.41±0.06a 19.41±0.22c 18.93±0.09b
球蛋白 GLOB/(g/L) 14.26±0.41bc 14.50±0.43c 14.08±0.19abc 13.48±0.37a 13.71±0.47ab
乳酸脱氢酶 LDH/(U/L) 94.36±0.48b 92.71±0.25a 95.14±0.26c 104.67±0.59e 97.43±0.22d
高密度脂蛋白胆固醇
HDL-C/(mmol/L)		 0.20±0.01c 0.20±0.01c 0.20±0.01c 0.15±0.01a 0.16±0.01b
低密度脂蛋白胆固醇
LDL-C/(mmol/L)		 0.22±0.01a 0.22±0.02a 0.24±0.01a 0.26±0.01b 0.27±0.01b
碱性磷酸酶 ALP/(U/L) 24.23±0.27b 23.29±0.19a 24.39±0.27b 26.32±0.30c 26.53±0.27c
葡萄糖 GLU/(mmol/L) 1.85±0.03b 1.72±0.03a 1.82±0.01b 2.05±0.07d 1.98±0.03c

2.5 不同蛋白质源替代鱼粉对牛蛙肝脏抗氧化指标的影响

由表7可知,B组和D组肝脏SOD、CAT活性及T-AOC与CK组无显著差异(P>0.05),但显著高于R组和C组(P<0.05);B组和D组肝脏MDA含量与CK组无显著差异(P>0.05),但显著低于R组和C组(P<0.05)。
表7 不同蛋白质源替代鱼粉对牛蛙肝脏抗氧化指标的影响

Table 7 Effects of different protein sources replacing fish meal on liver antioxidant indices of bullfrog (Aquarana catesbeiana)

项目
Items		 组别 Groups
CK B D R C
超氧化物歧化酶
SOD/(U/mg prot)		 10.51±0.06b 10.58±0.32b 10.26±0.14b 8.62±0.12a 8.73±0.18a
丙二醛 MDA/(nmol/mg prot) 1.52±0.04a 1.53±0.07a 1.57±0.03a 1.96±0.05b 1.92±0.03b
过氧化氢酶 CAT/(U/mg prot) 1.65±0.04bc 1.67±0.03c 1.61±0.04b 1.52±0.01a 1.51±0.02a
总抗氧化能力
T-AOC/(mmol/g prot)		 0.24±0.01b 0.24±0.01b 0.24±0.01b 0.20±0.01a 0.20±0.01a

2.6 不同蛋白质源替代鱼粉对牛蛙肝脏形态结构的影响

如图1所示,各组牛蛙肝脏均未观察到明显损伤。
图1 不同蛋白质源替代鱼粉对牛蛙肝脏形态结构的影响

CK、B、D、R和C分别表示CK组、B组、D组、R组和C组。图2同。

Fig.1 Effects of different protein sources replacing fish meal on liver morphological structure of bullfrog (Aquarana catesbeiana)

CK, B, D, R and C represented CK group, B group, D group, R group and C group, respectively. The same as Fig.2.

2.7 不同蛋白质源替代鱼粉对牛蛙肠道形态结构的影响

由表8可知,各替代组肠道绒毛高度与CK组无显著差异(P>0.05),B组肠道绒毛高度显著高于R组(P<0.05);B组和D组肠壁厚度与CK组无显著差异(P>0.05),但显著高于R组和C组(P<0.05)。牛蛙肠道组织切片染色结果(图2)显示,CK组、B组、D组和R组肠道绒毛结构较为完整、排列密集且长度较长,柱状上皮细胞排列整齐;而C组肠道出现上皮细胞自溶现象,且柱状上皮细胞排列不规则。
表8 不同蛋白质源替代鱼粉对牛蛙肠道绒毛高度和肠壁厚度的影响

Table 8 Effects of different protein sources replacing fish meal on intestinal villus height and intestinal wall thickness of bullfrog (Aquarana catesbeiana)μm

项目
Items		 组别 Groups
CK B D R C
绒毛高度 Villus height 514.84±8.36ab 516.24±7.09b 506.64±9.01ab 500.91±2.97a 502.00±8.53ab
肠壁厚度 Intestinal wall thickness 104.29±7.91b 103.78±3.93b 99.18±5.10b 87.45±4.01a 88.85±5.22a
图2 不同蛋白质源替代鱼粉对牛蛙肠道形态结构的影响

VH:绒毛高度 villus height;WT:肠壁厚度 intestinal wall thickness。

Fig.2 Effects of different protein sources replacing fish meal on intestinal morphological structure of bullfrog (Aquarana catesbeiana)

3 讨论

3.1 不同蛋白质源替代鱼粉对牛蛙生长性能的影响

生长性能可反映水产动物的营养状况[26]。研究表明,在肉食性鱼类饲料中使用植物蛋白质源替代鱼粉,通常会导致其生长速度减缓、饲料系数升高以及蛋白质利用效率下降[12]。另有研究发现,用豆粕和花生粕替代凡纳滨对虾饲料中40%以上的鱼粉时,其生长性能和饲料利用效率显著降低[27];用菜籽粕替代青鱼(Mylopharyngodon piceus)[28]饲料中30%以上或真鲷(Pagrus major)[29]饲料中37.5%以上的鱼粉,均明显抑制其生长;用棉籽粕替代乌苏拟鲿鱼(Pseudobagrus ussuriensis)[30]饲料中25.3%以上或鲤鱼[31]饲料中36%及以上的鱼粉时,同样显著降低生长性能。本研究结果表明,用棉籽粕或菜籽粕替代牛蛙饲料中37.5%的鱼粉,也会导致其生长性能降低和饲料系数提高,与多数已有研究结果一致。这可能与植物蛋白质源中抗营养因子和纤维素的存在[32-34],以及脂肪酸组成不平衡、缺乏胆固醇等重要营养素有关[35-37]。本研究结果还表明,用黑水虻干虫替代牛蛙饲料中37.5%的鱼粉,对其生长性能和饲料利用效率无显著影响,这与用黑水虻幼虫粉替代河蟹(Eriocheir sinensis)饲料中40%的鱼粉不影响其生长的结果[38]相似。此外,本研究中以脱脂黑水虻干虫替代37.5%的鱼粉,对牛蛙生长性能和饲料利用效率亦无显著影响,这与周琳[22]用脱脂黑水虻替代牛蛙幼蛙饲料中部分或全部鱼粉对其生长性能和饲料利用效率均无显著影响的研究结果相似。棉籽粕和菜籽粕替代鱼粉的效果劣于黑水虻干虫和脱脂黑水虻干虫,可能与黑水虻幼虫粉的优良消化特性有关——该虫粉中约78%的蛋白质可在胃蛋白酶-胰蛋白酶复合体系中被高效水解,消化速率较常规植物蛋白质提升20%~25%[39]。

3.2 不同蛋白质源替代鱼粉对牛蛙屠宰性能和肉品质的影响

肝胆综合征以肝胆肿大、变色为典型症状[40],其发生与饲料营养成分密切相关。本研究发现,与CK组相比,不同蛋白质源替代鱼粉对牛蛙肝体比、脏体比、净肉率和后腿肉率均无显著影响;但植物蛋白质源替代组(R组和C组)的肝体比较CK组有所提高,而昆虫蛋白质源替代组(B组和D组)的肝体比较CK组有所降低。这一结果提示,植物蛋白质源替代鱼粉可能对牛蛙肝脏健康产生一定负面影响,推测与其中抗营养因子的负面作用有关[41-42];而黑水虻干虫及脱脂黑水虻干虫替代鱼粉则对牛蛙肝脏健康具有一定保护作用,这可能得益于其含有的月桂酸、几丁质、抗菌肽等活性物质,这类物质可提高水产动物的抗氧化能力和免疫力[43]。此外,不同蛋白质源替代鱼粉均未对牛蛙的净肉率造成显著影响。肌肉pH及肉色是评价肉品质的基本指标[44],直接关系到产品的加工特性和市场接受度。其中,pH过高会影响肌肉加工成熟后的品质[45];肉色则是消费者直观判断肉制品优劣的重要依据,主要通过L*、a*和b*值进行量化评价,其中L*值与光照条件、肌肉表面水分含量及肉色饱和度密切相关[46]。本研究发现,各组牛蛙后腿肌肉pH及L*值均无显著差异,表明本研究所用不同蛋白质源替代部分鱼粉,不会影响牛蛙肌肉的加工品质及肉色饱和度。已有研究表明, a*和b*值的高低与肌肉氧化程度呈正相关[47]。本研究中,植物蛋白质源替代鱼粉组牛蛙后腿肌肉a*和b*值较CK组显著提高,提示植物蛋白质源替代鱼粉可能会增加牛蛙后腿肌肉氧化变质的风险。

3.3 不同蛋白质源替代鱼粉对牛蛙血清生化指标的影响

血清生化指标可反映动物机体生理代谢水平、营养状况及健康状态[48]。其中,血清ALB含量升高通常与内脏功能受损及相关疾病的发生有关[49];TG和CHO含量可反映机体脂肪代谢及脂质沉积状况[50];HDL-C和LDL-C则在机体CHO代谢方面发挥着重要作用[51]。本研究结果表明,B组和D组血清ALB含量与CK组无显著差异,而R组和C组血清ALB含量较CK组显著提高,说明用植物蛋白质源替代37.5%的鱼粉可能导致牛蛙内脏功能出现一定程度的损伤。同时,R组和C组血清LDL-C含量显著高于CK组,血清HDL-C含量显著低于CK组,说明用植物蛋白质源替代37.5%的鱼粉会干扰牛蛙机体CHO代谢,这与在青鱼[28]和杂交鲟(Acipenser schrenckii♀×Acipenser baerii♂)[52]饲料中用菜籽粕替代鱼粉后血清TG和CHO含量随替代比例升高呈降低趋势的研究结果相似。ALT和AST在肝脏氨基酸代谢和机体蛋白质代谢中起重要作用[53],而血液中ALT和AST活性升高通常与肝脏功能受损有关[54]。本研究结果表明,与CK组相比,R组和C组血清ALT和AST活性显著提高,说明植物蛋白质源替代37.5%的鱼粉对牛蛙肝脏组织完整性具有一定危害。这与菜籽粕替代青鱼饲料中30%以上鱼粉时,其血清AST和ALT活性显著上升的研究结果[28]一致;同时也与罗非鱼研究中随菜籽粕替代鱼粉比例增加,其血清AST和ALT活性显著提高的研究结果[55]相符。

3.4 不同蛋白质源替代鱼粉对牛蛙肝脏抗氧化指标的影响

动物机体抗氧化系统主要由抗氧化酶和非酶类抗氧化物质构成[56]。其中,SOD和CAT等酶在水产动物体内具有关键作用,能够有效降低氧化应激损伤[57-59]。T-AOC作为综合评价机体抗氧化性能的指标,能全面反映机体应对氧化应激的能力[60-61]。而MDA则对细胞具有毒性作用[62],其含量高低可反映细胞的受损程度。本研究中,用黑水虻干虫及脱脂黑水虻干虫替代37.5%的鱼粉对牛蛙肝脏抗氧化性能未产生负面影响,且用黑水虻干虫替代鱼粉可在一定程度上提高肝脏CAT和SOD活性,这与用黑水虻幼虫粉替代鱼粉饲喂黄颡鱼可提高其机体抗氧化性能的研究结果[63]相似。这一效果可能归因于黑水虻中含有的抗菌肽、几丁质及月桂酸等活性成分。研究表明,给虹鳟鱼饲喂含有抗菌肽富集型黑水虻幼虫(通过植物乳杆菌处理获得)的饲料,其免疫性能得到了改善[64];蝇蛆几丁质具有调节血脂、增强机体免疫调节功能的作用[65];月桂酸则具备较强的抗菌活性[66],且可通过调节肠道微生物改善水产机体健康状态[67]。本研究结果表明,用植物蛋白质源替代鱼粉显著降低了牛蛙肝脏抗氧化性能,这与丁李[68]的研究结果相符,其发现用豆粕替代牛蛙饲料中的鱼粉,会导致牛蛙体内促炎细胞因子mRNA相对表达量显著上调。综合来看,采用黑水虻干虫和脱脂黑水虻干虫替代牛蛙饲料中37.5%的鱼粉,对牛蛙的生理代谢、抗氧化功能及肝脏健康均未产生不良影响;而使用植物蛋白质源(菜籽粕和棉籽粕)进行相同比例的替代,则会产生不同程度的负面效应。

3.5 不同蛋白质源替代鱼粉对牛蛙肝脏和肠道形态结构的影响

本研究结果表明,各组牛蛙的肝脏组织形态均未出现明显异常,表明采用不同蛋白质源替代饲料中37.5%的鱼粉未对牛蛙肝脏组织形态造成明显损伤。这一结果与用脱脂黑水虻替代中华鳖饲料中30%的鱼粉不影响其肝脏组织形态的研究结果[69]相似。但胡俊茹等[53]研究发现,用黑水虻幼虫粉替代花鲈(Lateolabrax japonicas)饲料中的鱼粉,随着替代比例上升肝细胞出现广泛胞浆疏松、溶解或空泡化;Xie等[70]研究指出,使用低酚棉籽蛋白替代30%以上鱼粉会导致梭子蟹(Portunus trituberculatus)肝小管空泡化,降低其营养物质利用率并阻碍生长;He等[71]亦报道,用棉籽浓缩蛋白替代大口黑鲈(Micropterus salmoides)饲料中18%的鱼粉可引起肝脏颜色变黄及部分肝细胞弥漫性脂质空泡化。上述研究结果的差异,可能与试验动物种类、食性特征、试验周期以及鱼粉替代比例等不同有关。肠道是水产动物营养物质消化吸收的主要场所,其健康与结构完整性对牛蛙的生长发育至关重要。本研究发现,用棉籽粕和菜籽粕替代鱼粉均使牛蛙肠道绒毛高度和肠壁厚度降低,这可能是由于牛蛙作为肉食性水产动物,对饲料中植物蛋白质源的耐受性有限,比例过高易引起肠道组织结构损伤[72-73]。此外,C组牛蛙肠道出现上皮细胞自溶现象,这可能与棉籽粕中含有的游离棉酚等抗营养因子有关,这类物质会对水产动物的肠道黏膜及消化道结构造成损害,破坏肠道上皮细胞的完整性[74-75]。

4 结论

在本试验条件下,用黑水虻干虫和脱脂黑水虻干虫替代饲料中37.5%的鱼粉,对牛蛙生长性能、血清生化指标、抗氧化能力及肠道形态结构均无不良影响,且对肝脏健康具有一定的保护作用。因此,黑水虻可作为优质的鱼粉替代蛋白质源,有效降低牛蛙饲料中鱼粉的用量。

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