中国水产科学  2025, Vol. 32 Issue (01): 48-59  DOI: 10.12264/JFSC2024-0248
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引用本文 

林路佳, 王岩. 大黄鱼网箱养殖重金属废物排放的定量评价[J]. 中国水产科学, 2025, 32(1): 48-59. DOI: 10.12264/JFSC2024-0248.
LIN LuJia, WANG Yan. Quantifying waste outputs of heavy-metals from large yellow croaker (Larimichthys crocea) farming and its ecological effects[J]. Journal of Fishery Sciences of China, 2025, 32(1): 48-59. DOI: 10.12264/JFSC2024-0248.

基金项目

国家重点研发计划项目(2020YFD0900803);舟山市科技计划项目(2019C81054).

作者简介

林路佳(1998‒),女,硕士,研究方向为海洋资源与环境. E-mail:zjullj@163.com

通信作者

通信作者:王岩,教授,研究方向为水域生态学、鱼类营养和可持续水产养殖模式. E-mail:ywang@zju.edu.cn

文章历史

收稿日期:2024-07-29
修改日期:2024-09-18
大黄鱼网箱养殖重金属废物排放的定量评价
林路佳,王岩,     
浙江大学海洋学院,浙江 舟山 316021
摘要:定量评价海水鱼类养殖的重金属废物排放量可为完善产业规划和养殖管理提供科学依据。本研究分析了从6个大黄鱼(Larimichthys crocea)网箱养殖实验中采集的48个配合饲料和144个全鱼样品的铁(Fe)、铜(Cu)、锰(Mn)、铬(Cr)、镉(Cd)和铅(Pb)含量,首次利用改进的营养学模型计算了大黄鱼重金属贮积效率和养殖废物排放量。研究结果表明:按从高到低的顺序,饲料重金属含量Mn (709.284 mg/kg)>Fe (175.154 mg/kg)>Cu (34.215 mg/kg)>Pb (7.339 mg/kg)>Cr (0.688 mg/kg)>Cd (0.413 mg/kg);大黄鱼体内重金属含量Fe (10.187 mg/kg)>Mn (2.392 mg/kg)>Cu (0.581 mg/kg)>Cr (0.464 mg/kg)>Cd (0.014 mg/kg)>Pb (0.013 mg/kg);大黄鱼重金属贮积效率Fe (6.36%)>Cr (5.71%)>Cd (4.58%)>Pb (2.90%)> Cu (1.75%)>Mn (0.35%);养殖重金属废物排放量Mn [0.9764 g/(kg鱼产量)]>Fe [0.1990 g/(kg鱼产量)]> Cu [0.0422 g/(kg鱼产量)]>Cr [0.0081 g/(kg鱼产量)]>Pb [0.0007 g/(kg鱼产量)]>Cd [0.0004 g/ (kg鱼产量)]。大黄鱼重金属含量同时受饲料重金属含量和重金属贮积效率影响,其中全鱼Fe和Cr含量受重金属贮积效率影响较大,全鱼Mn、Cu、Pb和Cd含量受饲料重金属含量影响较大。大黄鱼养殖Fe、Cu、Mn废物排放量与养殖N和P废物排放量均显著正相关,表明养殖废物排放的Fe、Cu、Mn量与N和P排放量同步增加。鉴于N、P和Fe是海洋浮游植物的限制性营养盐,本研究初步推测大黄鱼离岸养殖可通过排放N、P和Fe增加海区的浮游植物生物量,进而提高初级生产力。
关键词大黄鱼养殖    重金属废物排放量    重金属贮积效率        食品安全    生态学效应    
Quantifying waste outputs of heavy-metals from large yellow croaker (Larimichthys crocea) farming and its ecological effects
LIN LuJia,WANG Yan    
Ocean College, Zhejiang University, Zhoushan 316021, China
Abstract:The quantitative evaluation of the heavy metal waste output from marine fish farming can provide scientific data for improving industrial planning and farming management of aquaculture. In this study, we analyzed contents of iron (Fe), copper (Cu), manganese (Mn), chromium (Cr), cadmium (Cd), and lead (Pb) in 48 samples of formulated feed and 144 samples large yellow croaker (Larimichthys crocea) whole-fish collected from six net-pen feeding trials, and determined the retention efficiency and waste outputs of the heavy-metals for the first time using a modified nutritional model that has been widely used for assessing nitrogen (N) and phosphorus (P) waste outputs of fish farming. The results showed that, the sequences were Mn (709.284 mg/kg)>Fe (175.154 mg/kg)> Cu (34.215 mg/kg)>Pb (7.339 mg/kg)>Cr (0.688 mg/kg)>Cd (0.413 mg/kg) for the content of the heavy-metals in the feed, Fe (10.187 mg/kg)>Mn (2.392 mg/kg)>Cu (0.581 mg/kg)>Cr (0.464 mg/kg)>Cd (0.014 mg/kg)>Pb (0.013 mg/kg) for the content of the heavy-metals in the whole-fish body, Fe (6.36%)>Cr (5.71%)>Cd (4.58%)>Pb (2.90%)>Cu (1.75%)>Mn (0.35%) for the retention efficiency of the heavy-metals, and Mn [0.9764 g/kg fish gain] >Fe [0.1990 g/kg fish gain] >Cu [0.0422 g/kg fish gain] >Cr [0.0081 g/kg fish gain] >Pb [0.0007 g/kg fish gain] >Cd [0.0004 g/kg fish gain] for the waste outputs of fish farming. The heavy-metal contents depended on either the heavy-metal content in the feed or the retention efficiency of the heavy metals. Fe and Cr in whole-fish bodies were mainly affected by retention efficiency of these elements, while contents of Mn, Cu, Pb, and Cd in whole-fish were mainly affected by the feed content of these elements. The waste outputs of Fe, Cu, and Mn significantly positively correlated to wastes of N and P, respectively, suggesting that the wastes of Fe, Cu, and Mn increased with the increase of wastes of N and P. Considering the critical roles of N, P, and Fe as the nutrients limiting growth of phytoplankton and primary productivity in ocean, the results indicated that waste outputs of offshore aquaculture of large yellow croaker could remarkably elevate biomass of phytoplankton and primary productivity in ocean.
Key wordslarge yellow croaker farming    waste output of heavy-metal    retention efficiency of heavy-metal    iron    food safety    ecological impact    

20世纪70年代至今,水产养殖产业一直处于快速发展中,同时投饵养殖在水产养殖产量中所占的比例也持续增加,现已超过70%[1]。投饵养殖不仅导致近海渔业资源(可作为饲料蛋白源)的过度捕捞[2-3],所产生的养殖废物还会导致水体富营养化[4-5],其对自然资源和环境的负面影响受到广泛关注[1-6]。有关水产养殖氮(N)和磷(P)废物排放量及其生态效应已有较多的研究[7-19],在养殖重金属排放方面,已有研究通过比较养殖和非养殖区域沉积物中重金属含量的差异,评价养殖活动的影响[20-22],但涉及养殖重金属废物排放的直接定量评价研究尚未见报道。铁(Fe)、铜(Cu)、锰(Mn)、铬(Cr)、镉(Cd)和铅(Pb)是环境中常见的重金属[23-28]。Fe、Cu和Mn参与构成超氧化物歧化酶[23],后者对清除生物体内活性氧自由基发挥重要作用;Cr参与构成动物葡萄糖耐量因子,后者参与调节动物糖和脂类代谢[24]。水产饲料原料中含有Fe、Cu、Mn、Cr、Cd和Pb等重金属,饲料添加剂中也加入一定量的Fe、Cu和Mn等以满足养殖动物的营养需求[29]。因此,投饵(配合饲料)养殖在产生N、P废物的同时也会产生重金属废物。Cd、Pb和Cr在较低浓度下即对水生生物具有毒性[26-28],而Fe、Cu和Mn当浓度超过阈值后也会产生负面影响[25],故定量评价水产养殖过程中Fe、Cu、Mn、Cr、Cd和Pb废物排放可为分析养殖活动对水生生物多样性和生态系统功能的影响提供数据,也可为完善产业规划和养殖管理提供科学依据。

大黄鱼是具有重要经济价值的海水鱼类种类,其养殖产量在海水鱼类中居世界第5位[1]、居我国第1位[30]。近年来,全程投喂配合饲料养殖大黄鱼技术取得突破[31-35],这将推动配合饲料在养殖生产中的应用,有助于进一步提高养殖产量。有关大黄鱼养殖的碳(C)、N和P废物排放量已有报道[32-35],但有关重金属废物排放方面的数据尚属匮乏。Song等[22]通过比较网箱养殖和非养殖海区沉积物中Cu、锌(Zn)、Cr、Cd、Pb和砷(As)含量的差异,评价了宁德三沙湾大黄鱼养殖的重金属污染。由于该研究未直接定量分析养殖排放的重金属量,故难以区分沉积物中的重金属受大黄鱼养殖或陆源污染的影响程度。N和P是海洋浮游植物的限制性营养盐[36]。近30年来,随着Fe假说的提出,Fe对海洋浮游植物生长和初级生产力的影响及其生物地球化学循环受到重视[37-39]。鱼类养殖过程中可同时以养殖废物的形式续排放N、P和Fe,其对区域性海洋浮游植物和初级生产力的影响是一个值得探究的问题。本研究提出了一种定量评价网箱养殖大黄鱼Fe、Cu、Mn、Cr、Cd和Pb等重金属废物排放量的方法,并初步探讨了重金属与N、P废物排放量的关系,旨在为明确大黄鱼养殖产业发展对沿岸带海洋生态系统的影响提供科学资料。

1 材料与方法 1.1 大黄鱼网箱养殖实验及配合饲料和实验鱼采样

2020—2021年在位于浙江省舟山市普陀区登步岛附近海域的优辰水产养殖合作社先后完成了6个网箱养殖实验,评价大黄鱼营养需求和饲料鱼粉替代潜力(表1)。所用大黄鱼为当年培育的鱼种,在1 m×1 m×2.5 m的网箱内养殖56~70 d,每个网箱内放养30~40尾鱼,初始体重为19.48~ 36.03 g。所用饲料为浙江大学水域生态系统与水产养殖实验室配方并制作的沉性配合饲料,饲料原料购自浙江德清生物科技有限公司。网箱实验期间每天5:00和17:00按饱食量投喂。网箱养殖实验中,测定了大黄鱼成活率、摄食率、生长(增重)、饲料利用效率(饲料系数以及饲料C、N、P和能量贮积效率)、全鱼组成(水分、粗蛋白、脂肪、灰分、磷、碳和能量含量)和养殖C、N和P废物排放量[32,34]

表1  大黄鱼网箱养殖实验时间和所用配合饲料的营养组成 Tab. 1  Duration of the net-pen feeding trials and nutrient composition of the experimental diets for large yellow croaker

养殖实验过程中对配合饲料随机采样,将其放入聚乙烯密封袋中并保存冰箱(−20 ℃)内。实验开始和结束时分别将鱼停喂24 h。实验开始时取3组鱼,单尾测量体长、体重后将鱼放入聚乙烯密封袋中并保存在冰箱(−20 ℃)内;实验结束时从每个网箱中取3尾鱼,测量体长、体重后保存在冰箱(−20 ℃)内。配合饲料和大黄鱼采样操作细节详见前文[32,34]。6个网箱养殖实验共采集配合饲料样品48个,大黄鱼全鱼样品144个。

1.2 样品分析

大黄鱼样品先在室温下解冻、称重。然后在LDZX-50KBS高压灭菌锅(上海申安医疗器械厂,中国)中蒸煮(121 ℃) 20 min、匀浆并烘干(105 ℃)。用小型高速粉碎机将烘干的饲料和大黄鱼样品粉碎并过80目筛,放入聚乙烯密封袋内并保存在干燥器中。采用国家标准方法(GB/T 5009)[40]测定饲料和大黄鱼的Fe、Cu、Mn、Cr、Cd和Pb含量。样品消解步骤如下:用MS104TS电子天平(0.01 mg/200 g, Mettler Toledo,瑞士)准确称取2.00000 g样品,放入石英坩埚内,坩埚使用前用1% HNO3 (优级纯)溶液浸泡、双蒸水清洗、烘干。待样品在通风橱内碳化至无烟后,将坩埚移入SX2-4-10N马弗炉(上海一恒科学仪器有限公司,中国)中灼烧(650 ℃) 7 h。向坩埚内加入20 mL 30%的HNO3 (优级纯)溶液使灰分完全溶解,然后将溶液转入50 mL容量瓶并用1% HNO3 (优级纯)溶液定容。Fe、Cu、Mn、Cr、Cd和Pb标准(浓度为1000 mg/L)购自中国有色金属及电子材料测试中心,稀释成使用液(浓度为20 μg/L)。用Thermo Fisher ICE 3500石墨炉原子吸收光谱(Thermo Fisher Scientific,美国)测定Fe、Cu、Mn、Cr、Cd和Pb含量。每个饲料和大黄鱼样品设2个重复,每个重复测定3次,取平均值作为测定结果。

1.3 数据计算和统计分析

确定水产养殖废物排放的方法包括系统收支方法[41]、水化学方法[42-43]和营养学方法[43]。系统收支方法根据养殖系统输入和输出物质的差异计算养殖废物积累量,需要测定整个养殖生产过程中所有输入和输出量,常用于估算某一养殖活动产生的污染[41]。水化学方法未考虑降雨、降尘、沉积和渗漏等的影响,常用于估算养殖废物在水中的积累情况[43]。营养学方法根据饲料摄入量和养殖动物体内贮积量计算养殖废物排放量,其原理是质量守恒,不仅准确度较高、容易操作,还可用于评价养殖过程中不同时间尺度上废物排放量的动态变化,被广泛用于水产养殖废物排放研究中[43-47]

Cho等[43]提出计算养殖废物排放量的营养学模型,该模型首先分别定量固体(SW)和溶解性(DW)养殖废物,再根据SW与DW计算总废物排放量。该模型中,SW=(被养殖动物摄食且消化吸收的营养物质–被养殖动物转化且贮存在体内的营养物质), DW=(投喂饲料中被养殖动物摄食的营养物质–被养殖动物摄食且消化吸收的饲料中营养物质+投喂但未被养殖动物摄食的饲料中的营养物质)。该模型需要分别单独计算SW和DW,实验操作不便,容易产生误差。为此,Wang等[9]对模型进行改进,直接计算总养殖废物排放量TW [TW=SW+DW=(投喂饲料中的营养物质−转化且贮存在养殖动物体内的营养物质)]。改进的模型先后被用于确定鮸状黄姑鱼[9]和点带石斑鱼[10]养殖的N废物排放量以及卵形鲳鲹[11-12]、花鲈[13]、日本黄姑鱼[14-15]、大口黑鲈[16-19]和大黄鱼[32-35]养殖的N、P废物排放量。

本研究中,利用Wang等[9]改进的模型计算养殖大黄鱼的Fe、Cu、Mn、Cr、Cd和Pb废物排放量。大黄鱼重金属贮积效率(MRE)和养殖废物排放量(MW)分别按下列公式计算:

MRE (%)=100%×(Wt/Nt×CMtW0/N0×CM0)/[2× I/(Nt+N0CMf]

MW [g/(kg鱼产量)]=1000×[2×I/(Nt+N0CMf / 100]×(1−MRE/100)/(Wt/NtW0/N0)

式中,I为实验期间每个网箱投喂的饲料量,单位为g; W0Wt分别为实验开始和结束时每个网箱内的实验鱼体重,单位均为g; N0Nt分别为实验开始和结束时每个网箱内实验鱼尾数;t为实验天数;CM0CMt分别为实验开始和结束时鱼体重金属含量百分比(%); CMf为饲料重金属含量百分比(%)。Fe、Cu、Mn、Cr、Cd和Pb的MRE分别用FeRE、CuRE、MnRE、CrRE、CdRE和PbRE表示,其MW分别用FeW、CuW、MnW、CrW、CdW和PbW表示。

实验数据表示为平均值±标准差($\bar x \pm {\rm{SD}}$)。利用成对数据t检验(Paired t-test)比较不同重金属之间分别在饲料含量、大黄鱼体含量、MRE和MW方面的差异。利用方差分析(ANOVA)和邓肯检验(Duncan’ test)分别比较同一实验中不同处理之间各个重金属的大黄鱼体含量、MRE和MW的差异。利用皮尔逊相关分析(Pearson correlation)检验MW与鱼生长以及养殖N、P废物排放量之间的关系,回归分析所用的大黄增重和养殖N、P废物排放量数据引用自相关网箱养殖实验(表1)的数据。t检验、方差分析、邓肯检验和回归分析利用SPSS 26.0软件完成,设差异显著性水平P为0.05;利用Origin 2021软件绘图。

2 结果与分析 2.1 配合饲料和大黄鱼体重金属含量

不同配合饲料以及投喂不同饲料的大黄鱼体Fe、Cu、Mn、Cr、Cd和Pb含量分别见图1图2。不同重金属之间在饲料含量和大黄鱼体含量方面均存在显著差异(P<0.05)。按平均值由高到低的顺序,饲料重金属含量依次为Mn [(709.284± 456.724) mg/kg, n=48]>Fe [(175.154±66.092) mg/kg, n=48]>Cu [(34.215±15.779) mg/kg, n=48]>Pb [(7.339±5.898) mg/kg, n=48]>Cr [(0.688±0.575) mg/kg, n=48]>Cd [(0.413±0.204) mg/kg, n=48];大黄鱼体重金属含量依次为Fe [(10.187±1.752) mg/kg, n=144]> Mn [(2.392±1.360) mg/kg, n=144]>Cu [(0.581± 0.514) mg/kg, n=144]>Cr [(0.464±0.116) mg/kg, n=144]>Cd [(0.014±0.011) mg/kg, n=144]>Pb [(0.013± 0.002) mg/kg, n=144]。

图1  实验饲料重金属含量Cr含量表示为测量值×10, Cu和Fe含量表示为测量@值×102, Mn含量表示为测量值×103. Fig. 1  Contents of the heavy metals in the experimental dietsThe contents of Cr, Fe and Cu were amplified by 10, 102, and 103, respectively.
图2  大黄鱼全鱼重金属含量Mn含量表示为测量值×10, Fe含量表示为测量值×102. Fig. 2  Contents of the heavy metals in whole-body of large yellow croakerThe contents of Mn and Fe were amplified by 10 and 102, respectively.

同一网箱实验中,不同饲料处理之间大黄鱼体Cr、Mn、Cd、Cu、Pb和Fe含量均表现出显著差异,具体情形因实验而异。实验1中,投喂饲料52P6L的鱼体Cr含量高于其他饲料处理(P<0.05),而投喂饲料43P6L的鱼体Mn含量高于其他饲料处理(P<0.05)。实验2中,投喂饲料BD的鱼体Cd和Cu含量分别高于其他饲料处理(P<0.05),投喂饲料F24和F16的鱼体Cr含量与投喂饲料SG24、SG16的鱼存在显著差异(P<0.05),投喂饲料SD16的鱼体Cr含量低于其他饲料处理(P<0.05)。实验3中,投喂饲料F40的鱼体Cd含量低于投喂低鱼粉饲料(F24、F16、F8)的鱼(P<0.05),投喂饲料F8的鱼体Pb含量高于其他饲料处理(P<0.05),投喂饲料F16D4的鱼体Mn含量高于其他饲料处理(P<0.05);实验4中,投喂饲料FM40的鱼体Fe含量高于投喂饲料FM32的鱼(P<0.05),后者高于投喂饲料FM24或FM16的鱼(P<0.05);鱼体Cr含量随饲料鱼粉含量降低而明显下降(P<0.05);投喂饲料FM40和FM32的鱼体Mn含量高于投喂饲料FM24和FM16的鱼(P<0.05);投喂饲料FMCN24的鱼体Fe含量高于其他饲料处理(P<0.05);投喂饲料FMCN24或FMCN16的鱼体Cu含量高于其他饲料处理(P<0.05)。实验5中,投喂饲料F16A3的鱼体Pb含量高于其他饲料处理(P<0.05)。实验6中,投喂饲料F24S0D1的鱼体Cu含量高于其他饲料处理(P<0.05)。

2.2 大黄鱼重金属贮积效率和养殖废物排放量

投喂不同饲料的大黄鱼MRE和MW分别见图3图4。所分析的6种重金属中,PbRE与CuRE之间无显著差异(P>0.05), CrRE与FeRE之间无显著差异(P>0.05),其余重金属的MRE之间均存在显著差异(P<0.05)。按平均值由高到低顺序,FeRE [(6.36±3.33)%, n=48]>CrRE [(5.71± 5.43)%, n=48]>CdRE [(4.58±3.93)%, n=48]> PbRE [(2.90±2.85)%, n=48]>CuRE [(1.75±1.72)%, n=48]>MnRE [(0.35±0.25)%, n=48]。不同重金属MW之间存在显著差异(P<0.05),从高到低依次为:Mn [(0.9764±0.8715) g/(kg鱼产量), n=48]>Fe [(0.1990±0.1012) g/(kg鱼产量), n=48]>Cu [(0.0422± 0.0217) g/(kg鱼产量), n=48]>Cr [(0.0081±0.0065) g/ (kg鱼产量), n=48]>Pb [(0.0007±0.0004) g/(kg鱼产量), n=48]>Cd [(0.0004±0.0001) g/(kg鱼产量), n=48]。

图3  大黄鱼对饲料重金属的贮积效率 Fig. 3  Retention efficiency of the heavy metals in large yellow croaker
图4  大黄鱼养殖重金属废物排放量Cr废物排放量表示为测量值×10, Pb和Cd废物排放量表示为测量值×102. Fig. 4  Waste outputs of the heavy metals from large yellow croaker farmingCr waste was amplified by 10, and wastes of Pb and Cd were amplified by 102.

同一网箱实验中,不同饲料处理之间Mn、Cu、Fe、Pb、Cr和Cd的MW均表现出显著差异,具体情形因实验而异。实验1中,投喂饲料43P6L的MnW高于其他饲料处理(P<0.05);投喂饲料52P12L的CuW和FeW高于其他饲料处理(P<0.05)。实验2中,投喂饲料BD的PbW、CrW、MnW和FeW高于其他饲料处理(P<0.05),投喂饲料FG16的CuW高于其他饲料处理(P<0.05)。实验3中,CrW和FeW随饲料鱼粉含量降低而明显下降(P<0.05);投喂饲料F16D8的PbW高于其他饲料处理(P<0.05);投喂饲料F16D12的CrW高于其他饲料处理(P<0.05);投喂饲料F16D4的CuW最低(P<0.05);投喂饲料F16D16的FeW高于其他饲料处理(P<0.05)。实验4中,CrW、MnW和FeW随饲料鱼粉含量降低而明显下降(P<0.05);投喂饲料FM40的PbW高于其他饲料处理(P<0.05);投喂饲料FM40或FM32的CrW高于投喂饲料FM24的废物排放量(P<0.05),后者高于投喂饲料FM16的废物排放量(P<0.05);投喂饲料FMN24的CdW和PbW高于其他饲料处理(P<0.05);投喂饲料FMC24或FMC16的CrW最高(P<0.05);投喂饲料FMCN16的MnW高于其他饲料处理(P<0.05);投喂饲料FMC24、FMN24和FMCN24的FeW高于投喂饲料FMC16、FMN16和FMCN16的FeW (P<0.05)。实验5中,投喂饲料F16A3的CdW、PbW、CdW、CuW、MnW和FeW均显著高于其他饲料处理(P<0.05)。实验6中,投喂饲料F24S0D1的PbW高于其他饲料处理(P<0.05);投喂饲料F24S3的CrW和CuW高于其他饲料处理(P<0.05);投喂饲料F24S4的MnW高于其他饲料处理(P<0.05)。

2.3 MW与大黄鱼生长以及养殖氮、磷废物排放量的关系

图5可见,FeW、CuW和CrW与大黄鱼增重(WG)显著正相关(P<0.05), MnW、CdW和PbW与WG显著负相关(P<0.05)。Fe、Cu、Mn和Cd废物排放量与N、P废物排放量均呈显著正相关(P<0.05), Pb废物排放量与P废物排放量显著正相关(P<0.05)。

图5  大黄鱼养殖中重金属废物排放量与增重(WG)及氮、磷废物排放量(NW和PW)之间的相关性圆点大小表示相关性系数的绝对值. |r|≥0.17时表示因子间显著相关(n=48, P<0.05).红色表示正相关,蓝色表示负相关. Fig. 5  Pearson’s correlation coefficients between weight gain (WG), wastes output of N or P (i.e., NW and PW) and wastes of heavy metals in large yellow croaker farmingThe size of points represent the absolute values of the correlation coefficients. The correlation was significant when |r|≥0.17 (n=48, P<0.05). Red represents positive correlation, and blue represents negative correlation.
3 讨论 3.1 大黄鱼养殖的重金属废物排放量

目前,有关水产养殖重金属污染的研究多采用分析沉积物重金属含量的方法。例如,Belias等[20]在Astakos湾内网箱养殖区域设置沉积物捕集器,通过分析收集的沉积物Cd、Fe、Cu、Zn等重金属含量评价鱼类网箱养殖重金属污染情况;Mendiguchia等[21]根据1997年2月和1998年3月对Cadiz湾内海水养殖区域表层沉积物中Zn、Cu、Pb含量的采样分析评价了养殖活动的影响。由于未直接定量养殖排放的重金属,这类研究往往难以确定沉积物重金属含量的变化是否完全由养殖活动引起,因此也难以准确评价养殖重金属废物排放对水域生态系统的影响。本研究第一次利用营养学模型定量评价鱼类养殖的重金属废物排放量。研究结果表明,大黄鱼养殖中排放最多的重金属元素是Mn,其次为Fe,再次为Cu;相比之下,Cr、Cd和Pb排放量较低。按2020年国内大黄鱼养殖产量(25.77万t)[30]推算,假如完全投喂配合饲料,该年度大黄鱼养殖将向海洋中排放251.63 t Mn、51.28 t Fe、10.88 t Cu、2.08 t Cr、0.11 t Cd和0.18 t Pb。

饲料蛋白质和脂肪含量[11,14,16]、饲料鱼粉替代水平[10,12,13,15,17,18,32-34]和投喂频率[9,35]等均可影响鱼类养殖的N、P废物排放量。本研究发现,饲料鱼粉替代水平和替代蛋白原料的种类可影响大黄鱼养殖的FeW、CuW、MnW、CrW、CdW和PbW。例如,以SPC为鱼粉替代蛋白源时,PbW、CrW和FeW随饲料鱼粉含量下降而减少;以PBM为鱼粉替代蛋白源时,CrW随饲料鱼粉含量下降而减少;投喂高鱼粉(400 g/kg)饲料养殖大黄鱼时FeW和CuW较高,投喂低鱼粉(80 g/kg)饲料时MnW和CuW较高。此外,本研究发现饲料配方中添加核苷酸、姜黄素和肠膜蛋白等功能性成分也会导致部分重金属废物排放量变化,造成这一现象的原因和机理尚不清楚,需要进一步的实验来验证和分析。

3.2 饲料中重金属在大黄鱼体内的积累

鱼体内重金属积累程度影响到鱼类健康和食品安全[25-26,48]。本研究中,大黄鱼全鱼Fe、Cu、Mn、Cr、Cd和Pb平均含量分别为10.187、0.581、2.392、0.464、0.014和0.013 mg/kg。杜冰等[49]报道大黄鱼肌肉Cu、Cr、Pb和Cd平均含量分别为0.312、0.020、0.008和0.009 mg/kg。齐自元等[50]报道大黄鱼肌肉Cr、Pb和Cd的平均含量分别为0.044、0.007和0.001 mg/kg。与上述研究[49-50]相比,本研究所报道的大黄鱼全鱼Cu、Cr、Pb和Cd含量均超过所报道的肌肉含量,研究中全鱼Cr含量超过所报道的肌肉含量的10倍,全鱼Cu和Pb含量约为肌肉含量的2倍。不同研究中大黄鱼体内重金属含量差异较大的原因一方面与分析的鱼体部位有关(不同器官和组织中重金属积累程度不同),另外还与鱼类食物来源和生活环境有关(重金属可通过食物链富集,故食物链中位于不同营养级的鱼类重金属积累程度不同)。本研究中,6种重金属在大黄鱼体内含量从高到低依次为:Fe>Mn>Cu>Cr>Cd>Pb。Cai等[51]报道贵州省乌江渡水库中7种淡水鱼类肌肉重金属含量从高到低依次为:Zn (10.765 mg/kg)>Fe (8.908 mg/kg)>Mn (0.373 mg/kg)>Cu (0.369 mg/kg)>Pb (0.158 mg/kg)> As (0.102 mg/kg)>Hg (0.042 mg/kg)>Cd (0.024 mg/kg),同样呈现鱼体Fe、Mn、Cu含量大于Pb和Cd含量的趋势。大黄鱼全鱼Fe、Mn、Cu平均含量明显高于乌江渡水库淡水鱼肌肉相应重金属含量,反映出鱼体内重金属积累程度与环境状况密切相关。

鱼体内总金属含量受食物重金属含量影响。研究发现,斜带石斑鱼(Epinephelus coioides) Cu含量随饲料Cu含量增加而显著增加[52];大口黑鲈Mn含量随饲料Mn含量增加而明显增加[53];增加饲料Fe含量导致牙鲆(Paralichthys olivaceu)幼鱼肝脏Fe含量显著增加[54],导致大西洋鲑(Salmo salar)全鱼Fe含量增加[55]。本研究中,饲料重金属含量从高到低依次为:Mn>Fe>Cu>Cr> Pb>Cd,而大黄鱼重金属含量从高到低依次为:Fe>Mn>Cu>Cr>Cd>Pb。同时,大黄鱼对重金属贮积效率从高到低依次为:FeRE>CrRE>PbRE> CdRE>CuRE>MnRE。大黄鱼体内重金属含量、饲料重金属含量和大黄鱼重金属贮积效率的高低次序并不完全一致,表明大黄鱼重金属含量不仅取决于饲料重金属含量,还取决于其对重金属的贮积效率。通过比较大黄鱼重金属含量、饲料重金属含量以及大黄鱼的重金属贮积效率的高低次序,初步判断:鱼体Fe和Cr含量同时取决于饲料重金属含量和重金属贮积效率,且后者的作用略大于前者;鱼体Mn、Cu、Pb和Cd含量主要取决于饲料重金属含量,重金属贮积效率发挥次要作用。Fe、Mn和Cu是鱼类生长和代谢所需的营养素[23],大黄鱼和饲料Fe、Mn和Cu含量相对较高,养殖废物排放量相对较大,表明这3种重金属是大黄鱼养殖中重金属废物排放管理的重点。大黄鱼Cu和Mn贮积效率较低,一方面可能与其饲料含量高有关,另一方面也可能与鱼对其代谢和排泄较快有关。相比之下,尽管大黄鱼和饲料Cd和Pb含量均较低,但其贮积效率高于Cu和Mn贮积效率,一旦饲料Pb和Cd含量升高,鱼体内这两种重金属将以较快的速度积累。因此,Cd和Pb对大黄鱼养殖食品安全的风险应大于对环境安全的风险。

3.3 大黄鱼养殖废物排放的潜在生态学效应

投饵养殖中,饲料内大部分的N、P以养殖废物的形式排放到环境中,对水域系统结构和功能产生影响[6]。研究表明大黄鱼对饲料N的贮积效率为15.23%~42.27%,对P的贮积效率为12.18%~ 52.83%[32-35]。本研究中,大黄鱼对饲料Mn、Fe、Cu、Cr、Pb和Cd的平均贮积效率分别为0.35%、6.36%、1.75%、5.71%、2.90%和4.58%,明显低于对饲料N和P的贮积效率[31-35]。这意味着饲料中的Mn、Fe、Cu、Cr、Pb和Cd超过90%以废物的形式排放;Fe、Mn和Cu废物排放量与N、P废物排放量均显著正相关,表明养殖废物中Fe、Cu和Mn与N和P数量同步增加。N、P以及Fe、Cu和Mn均为浮游植物生长和代谢必需的营养素。本研究涉及的网箱养殖实验(表1)结果表明投喂配合饲料养殖大黄鱼时N和P废物排放量分别为71.26 g N/(kg鱼产量)和15.90 g P/(kg鱼产量)[31-32,34], N/P为10,据此计算大黄鱼养殖废物的Fe/P、Mn/P和Cu/P分别为6.9×10–3、3.5×10–2和1.3×10–3。大洋中Fe/C为1×10–5~1×10–4[37],按C/P为106推算,Fe/P为1.06×10–7~1.06×10–6。相比之下,大黄鱼养殖废物的Fe/P高于大洋海水中的Fe/P,约为后者的6倍。这意味着大黄鱼养殖废物排放有益于缓解Fe缺乏对海洋浮游植物生长和初级生产力的限制作用。根据本研究结果,在气候变暖导致海洋层化加剧,海洋初级生产力因营养盐限制而趋于下降的全球背景下[56],合理发展离岸海水鱼类养殖不仅有利于满足人类对高质量动物性食品蛋白的需求,还可通过持续释放N、P和Fe提高海洋初级生产力,增强海洋渔产力和碳汇。这一推测有待实验验证。此外,海洋浮游植物对Fe的利用与其存在形态有关,而本研究仅仅确定了鱼类养殖废物Fe的总量,有关可溶性Fe,特别是生物可利用Fe在养殖Fe废物中所占的比例还需要进一步研究。

4 结论

按从高到低次序,大黄鱼网箱养殖重金属废物排放量依次为:Mn>Fe>Cu>Cr>Pb>Cd;大黄鱼重金属含量依次为:Fe>Mn>Cu>Cr>Cd>Pb,全鱼重金属含量取决于饲料重金属含量及其贮积效率。大黄鱼养殖的Fe、Mn和Cu养殖废物排放量与N、P废物排放量正相关,表明养殖N、P和Fe废物排放可对海洋浮游植物产生协同影响,有助于增加浮游植物生物量和提高初级生产力。

参考文献
[1]
FAO. The state of world fisheries and aquaculture 2022[R]. Rome: FAO, 2022: 1-40..》Google Scholar
[2]
Naylor R L, Goldburg R J, Primavera J H, et al. Effect of aquaculture on world fish supplies[J]. Nature, 2000, 405: 1017-1024..》Google Scholar
[3]
Naylor R L, Hardy R W, Buschmann A H, et al. A 20-year retrospective review of global aquaculture[J]. Nature, 2021, 591: 551-563..》Google Scholar
[4]
Luo Z B, Hu S Y, Chen D J. The trends of aquacultural nitrogen budget and its environmental implications in China[J]. Scientific Reports, 2018, 8(1): Article No.10877..》Google Scholar
[5]
Kong W W, Huang S L, Yang Z J, et al. Fish feed quality is a key factor in impacting aquaculture water environment: Evidence from incubator experiments[J]. Scientific Reports, 2020, 10: 187..》Google Scholar
[6]
Edwards P. Aquaculture environment interactions: Past, present and likely future trends[J]. Aquaculture, 2015, 447: 2-14..》Google Scholar
[7]
Mallekh R, Boujard T, Lagardère J P. Evaluation of retention and environmental discharge of nitrogen and phosphorus by farmed turbot (Scophthalmus maximus)[J]. North American Journal of Aquaculture, 1999, 61(2): 141-145..》Google Scholar
[8]
Paspatis M, Boujard T, Maragoudaki D, et al. European sea bass growth and N and P loss under different feeding practices[J]. Aquaculture, 2000, 184(1-2): 77-88..》Google Scholar
[9]
Wang Y, Kong L J, Li K, et al. Effects of ration level and feeding frequency on growth, feed utilization and carcass composition of cuneate drum (Nibea miichthioides) reared in net pens[J]. Aquaculture, 2007, 271(1-4): 350-356..》Google Scholar
[10]
Wang Y, Li K, Han H, et al. Potential of using a blend of rendered animal protein ingredients to replace fish meal in practical diets for malabar grouper (Epinephelus malabricus)[J]. Aquaculture, 2008, 281(1-4): 113-117..》Google Scholar
[11]
Wang F, Han H, Wang Y, et al. Growth, feed utilization and body composition of juvenile golden pompano Trachinotus ovatus fed at different dietary protein and lipid levels[J]. Aquaculture Nutrition, 2013, 19(3): 360-367..》Google Scholar
[12]
Wang Y, Ma X Z, Wang F, et al. Supplementations of poultry by-product meal and selenium yeast increase fish meal replacement by soybean meal in golden pompano (Trachinotus ovatus) diet[J]. Aquaculture Research, 2017, 48(4): 1904-1914..》Google Scholar
[13]
Wang Y, Wang F, Ji W X, et al. Optimizing dietary protein sources for Japanese sea bass (Lateolabrax japonicus) with an emphasis on using poultry by-product meal to substitute fish meal[J]. Aquaculture Research, 2015, 46(4): 874-883..》Google Scholar
[14]
Chai X J, Ji W X, Han H, et al. Growth, feed utilization, body composition and swimming performance of giant croaker, Nibea japonica Temminck and Schlegel, fed at different dietary protein and lipid levels[J]. Aquaculture Nutrition, 2013, 19(6): 928-935..》Google Scholar
[15]
Wu Y B, Ren X, Chai X J, et al. Replacing fish meal with a blend of poultry by-product meal and feather meal in diets for giant croaker (Nibea japonica)[J]. Aquaculture Nutrition, 2018, 24(3): 1085-1091..》Google Scholar
[16]
Huang D, Wu Y B, Lin Y Y, et al. Dietary protein and lipid requirements for juvenile largemouth bass, Micropterus salmoides[J]. Journal of the World Aquaculture Society, 2017, 48(5): 782-790..》Google Scholar
[17]
Wang L, Cui Z H, Ren X, et al. Growth performance, feed cost and waste outputs of largemouth bass Micropterus salmoides fed low fish meal diets[J]. Aquaculture Reports, 2021, 20: 100757..》Google Scholar
[18]
Cui Z H, Zhang J Y, Ren X, et al. Replacing dietary fish meal improves ecosystem services of largemouth bass (Micropterus salmoides) farming[J]. Aquaculture, 2022, 550: 737830..》Google Scholar
[19]
Cui Z H, Yu C, Li Y M, et al. Effect of fermented brewer’s yeast (Saccharomyces cerevisiae) supplementation on growth, feed utilization, and water quality in largemouth bass (Micropterus salmoides) farming[J]. Journal of Fishery Sciences of China, 2022, 29(2): 274-283. [崔正贺,余聪,李云梦,等. 饲料中发酵啤酒酵母添加水平对大口黑鲈生长,饲料利用效率和水质的影响[J]. 中国水产科学,2022, 29(2): 274-283.].》Google Scholar
[20]
Belias C V, Bikas V G, Dassenakis M J, et al. Environmental impacts of coastal aquaculture in eastern Mediterranean Bays: The case of Astakos Gulf, Greece[J]. Environmental Science and Pollution Research, 2003, 10(5): 287-295..》Google Scholar
[21]
Mendiguchía C, Moreno C, Mánuel-Vez M P, et al. Preliminary investigation on the enrichment of heavy metals in marine sediments originated from intensive aquaculture effluents[J]. Aquaculture, 2006, 254(1-4): 317-325..》Google Scholar
[22]
Song Y, Li M T, Fang Y X, et al. Effect of cage culture on sedimentary heavy metal and water nutrient pollution: Case study in Sansha Bay, China[J]. Science of the Total Environment, 2023, 899: 165635..》Google Scholar
[23]
Jomova K, Makova M, Alomar S Y, et al. Essential metals in health and disease[J]. Chemico-Biological Interactions, 2022, 367: 110173..》Google Scholar
[24]
Schwarz K, Mertz W. Chromium (III) and the glucose tolerance factor[J]. Archives of Biochemistry & Biophysics, 1959, 85(1): 292-295..》Google Scholar
[25]
Shahjahan M, Taslima K, Rahman M S, et al. Effects of heavy metals on fish physiology-A review[J]. Chemosphere, 2022, 300: 134519..》Google Scholar
[26]
Kamila S, Shaw P, Islam S, et al. Ecotoxicology of hexavalent chromium in fish: An updated review[J]. Science of the Total Environment, 2023, 890: 164395..》Google Scholar
[27]
Friberg L J, Piscator M, Nordberg G F, et al. Cadmium in the Environment[M]. Carabas: CRC Press, 1974: 1-260..》Google Scholar
[28]
García-Lestón J, Méndez J, Pásaro E, et al. Genotoxic effects of lead: An updated review[J]. Environment International, 2010, 36(6): 623-636..》Google Scholar
[29]
Hertrampf J W, Piedad-Pascual F. Handbook on Ingredients for Aquaculture Feeds[M]. Dordrecht: Kluwer Academic Publishers, 2000: 1-573..》Google Scholar
[30]
Administrative Department for Fisheries of Ministry of Agriculture and Rural Affairs of PRC, National Fisheries Technology Extension Center, China Society of Fisheries. China Fishery Statistical Yearbook 2021[M]. Beijing: China Agriculture Press, 2021: 1-180. [中华人民共和国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. 2021中国渔业统计年鉴[M]. 北京:中国农业出版社,2021: 1-180.].》Google Scholar
[31]
Chen Z M, Yu A L, Wang L, et al. Reassessment of dietary protein and lipid requirements for large yellow croaker, Larimichthys crocea, reared in net pens[J]. Journal of the World Aquaculture Society, 2023, 54(5): 1179-1195..》Google Scholar
[32]
Chen Z M, Ibrahim U B, Yu A L, et al. Dried porcine soluble benefits to increase fish meal replacement with soy protein concentrate in large yellow croaker Larimichthys crocea diet[J]. Journal of the World Aquaculture Society, 2023, 54(5): 1162-1178..》Google Scholar
[33]
Yu A L, Wang L, Chen Z M, et al. Influences of keratinase DP-100 and gamma irradiation on feather meal as a fish meal substitute in large yellow croaker diet[J]. Journal of Fishery Sciences of China, 2023, 30(5): 630-642. [于安澜,王力,陈子末,等. 角蛋白酶DP-100和γ射线辐照对利用羽毛粉替代大黄鱼饲料鱼粉的影响[J]. 中国水产科学,2023, 30(5): 630-642.].》Google Scholar
[34]
Wang L, Lei M T, Yu A L, et al. Dried porcine soluble augments dietary fishmeal replacement by poultry by-product meal for large yellow croaker Larimichthys crocea[J]. Aquaculture, 2024, 593: 741306..》Google Scholar
[35]
Liu Y, Lei M T, Victor H, et al. The optimal feeding regime for large yellow croaker Larimichthys crocea, with an emphasis on obviating raw fish diet in commercial farming[J]. Aquaculture, 2024, 580: 740293..》Google Scholar
[36]
Hecky R E, Kilham P. Nutrient limitation of phytoplankton in freshwater and marine environments: A review of recent evidence on the effects of enrichment[J]. Limnology and Oceanography, 1988, 33(4): 796-822..》Google Scholar
[37]
Martin J H. Glacial-interglacial CO2 change: The iron hypothesis[J]. Paleoceanography, 1990, 5(1): 1-13..》Google Scholar
[38]
Boyd P W, Watson A J, Law C S, et al. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization[J]. Nature, 2000, 407: 695-702..》Google Scholar
[39]
Tagliabue A, Bowie A R, Boyd P W, et al. The integral role of iron in ocean biogeochemistry[J]. Nature, 2017, 543: 51-59..》Google Scholar
[40]
Ministry of Health of the People's Republic of China, Standardization Administration of the People's Republic of China. Methods of food hygienic analysis: Physical and chemical section-general principles: GB/T 5009.1-2003[S] Beijing: Standards Press of China, 2003. [中华人民共和国卫生部,中国国家标准化管理委员会. 食品卫生检验方法理化部分:GB/T 5009.1-2003[S]. 北京:中国标准出版社,2003.].》Google Scholar
[41]
Green B W, Boyd C E. Chemical budgets for organically fertilized fish ponds in the dry tropics[J]. Journal of the World Aquaculture Society, 1995, 26(3): 284-296..》Google Scholar
[42]
Roque d'Orbcastel E, Blancheton J P, Boujard T, et al. Comparison of two methods for evaluating waste of a flow through trout farm[J]. Aquaculture, 2008, 274(1): 72-79..》Google Scholar
[43]
Cho C Y, Hynes J D, Wood K R, et al. Quantitation of fish culture wastes by biological (nutritional) and chemical (limnological) methods; the development of high nutrient dense (HND) diets[B]. In: Nutritional Strategies and Aquaculture Waste. Proceedings of the 1st International Symposium on Nutritional Strategies in Management of Aquaculture Waste (ed. by Cowey C B and Cho C Y), 1991, 37-50. University of Guelph, Ontario, Canada..》Google Scholar
[44]
Cho C Y, Hynes J D, Wood K R, et al. Development of high-nutrient-dense, low-pollution diets and prediction of aquaculture wastes using biological approaches[J]. Aquaculture, 1994, 124(1-4): 293-305..》Google Scholar
[45]
Cho C Y, Bureau D P. Development of bioenergetic models and the Fish-PrFEQ software to estimate production, feeding ration and waste output in aquaculture[J]. Aquatic Living Resources, 1998, 11(4): 199-210..》Google Scholar
[46]
Bureau D P, Gunther S J, Cho C Y. Chemical composition and preliminary theoretical estimates of waste outputs of rainbow trout reared in commercial cage culture operations in Ontario[J]. North American Journal of Aquaculture, 2003, 65(1): 33-38..》Google Scholar
[47]
Bureau D P, Hua K. Towards effective nutritional management of waste outputs in aquaculture, with particular reference to salmonid aquaculture operations[J]. Aquaculture Research, 2010, 41(5): 777-792..》Google Scholar
[48]
Bosch A C, O’Neill B, Sigge G O, et al. Heavy metals in marine fish meat and consumer health: A review[J]. Journal of the Science of Food & Agriculture, 2016, 96(1): 32-48..》Google Scholar
[49]
Du B, Sun L M, Hao W B, et al. Concentration and risk assessment of heavy metals in aquatic products collected from Taiwan shallow fishery[J]. Journal of Agro-Environment Science, 2016, 35(11): 2049-2058. [杜冰,孙鲁闽,郝文博,等. 台海浅滩渔场不同水产品中重金属含量与暴露风险评价[J]. 农业环境科学学报,2016, 35(11): 2049-2058.].》Google Scholar
[50]
Qi Z Y, Cao H, Hu Y M, et al. Differences and risk assessment of heavy metals in seafood and freshwater products[J]. Journal of Fisheries of China, 2022, 46(7): 1246-1256. [齐自元,曹欢,胡钰梅,等. 海产品与淡水产品中重金属的差异性及其风险评价[J]. 水产学报,2022, 46(7): 1246-1256.].》Google Scholar
[51]
Cai S W, Zeng B P, Li C T. Potential health risk assessment of metals in the muscle of seven wild fish species from the Wujiangdu reservoir, China[J]. Quality Assurance and Safety of Crops & Foods, 2023, 15(1): 73-83..》Google Scholar
[52]
Ye C X, Liu Y J, Tian L X, et al. Effects of elevated dietary copper levels on growth and Cu, Fe, Mn, Zn content of juvenile grouper Epinephelus coioides[J]. Oceanlogia et Limnologia Sinica, 2013, 44(3): 606-610. [叶超霞,刘永坚,田丽霞,等. 饲料中高水平铜对斜带石斑鱼(Epinephelus coioides)生长和铜、铁、锰、锌含量的影响[J]. 海洋与湖沼,2013, 44(3): 606-610.].》Google Scholar
[53]
Song B W, Yang H, Leng X J, et al. Dietary requirement of Mn for juvenile largemouth bass (Micropterus salmoides)[J]. Journal of Fisheries of China, 2023, 47(5): 153-161. [宋博文,杨航,冷向军,等. 大口黑鲈幼鱼对饲料中锰的需求量[J]. 水产学报,2023, 47(5): 153-161.].》Google Scholar
[54]
Wei W Q, Li A J, Li D S, et al. Effect of dietary supplemented iron on growth of the juvenile flounder Paralichthys olivaceu[J]. Journal of Fisheries of China, 1999, 23(S1): 100-103. [魏万权,李爱杰,李德尚,等. 饲料中添加铁对牙鲆幼鱼生长的影响[J]. 水产学报,1999, 23(S1): 100-103.].》Google Scholar
[55]
Maage A, Sveier H, Julshamn K. A comparison of growth rate and trace element accumulation in Atlantic salmon (Salmo salar) fry fed four different commercial diets[J]. Aquaculture, 1989, 79(1-4): 267-273..》Google Scholar
[56]
Moore J K, Fu W W, Primeau F, et al. Sustained climate warming drives declining marine biological productivity[J]. Science, 2018, 359(6380): 1139-1143..》Google Scholar