富营养条件下水培旱柳对锌和铜的富集特性
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摘要
以旱柳(Salix matsudana Koidz)为研究对象,采用水培方法,研究富营养化条件下重金属污染对旱柳的生长特性、生理指标以及重金属富集的影响.结果表明:50μmol/L铜(Cu)处理会显著抑制旱柳生长并引起相应的生理活动,表现为干重、相对生长速率(RGR)、耐性指数(TI)及光合色素含量降低,丙二醛(MDA)含量和过氧化物酶(POD)活性升高,且50μmol/L Cu对旱柳的毒害远大于50μmol/L锌(Zn).随着氮(N)、磷(P)浓度提高,旱柳生物量提高,MDA含量和POD活性降低,重金属对旱柳的毒害得到缓解.Cu和Zn主要富集在旱柳根部(插条新生根,下同),但随着N、P浓度的提高,旱柳根部富集Cu和Zn的量显著减少. Cu会增加旱柳根部对Zn的富集,显著降低Zn的转运系数,抑制Zn向新生枝条转运. 3种N、P组合(N0+P0、N1.5+P0.18和N15+P1.8,下同)下,与Zn50处理相比,Zn50+Cu50处理下Zn转运系数分别显著降低了62.8%、57.0%和77.9%(P <0.05);Zn会减少旱柳根部对Cu的富集,显著提高Cu的转运系数,促使Cu向新生枝条部转运.3种N、P组合下,与添加Cu50的处理相比,Zn50+Cu50处理下Cu的转运系数分别显著提高了26.0%、62.9%和42.9%(P <0.05). N、P浓度的提高会促使Zn向新生枝条部转运,与N0+P0+Zn50相比,N1.5+P0.18+Zn50和N15+P1.8+Zn50处理下Zn的转运系数分别显著提高了45.6%和247.3%(P <0.05),而对Cu的转运无显著影响.综上,旱柳插条对Cu和Zn具有很强的富集能力,N、P浓度的提高可在一定程度上缓解重金属对旱柳的毒害,减少新生根对Cu和Zn的富集并促使Zn向新生枝条转运.(图9表2参38)
The effect of heavy metal pollution on growth characteristics, physiological indexes, and heavy metal accumulation was explored under eutrophication conditions using hydroponically growing Salix matsudana cuttings. The results showed that under the 50 μmol/L Cu treatment condition, cutting growth was significantly inhibited and the physiological response to stunted growth was induced, with decreasing dry weight, RGR, tolerance index(TI), and amount of photosynthetic pigment,as well as increasing MDA content and POD activity. The damage, as a result of 50 μmol/L Cu treatment in S. matsudana was more serious than that with 50 μmol/L Zn treatment. With the increase in N and P concentration, biomass increased while MDA content and POD activity decreased. Eutrophication could alleviate the damage caused by heavy metals on S. matsudana.Cu and Zn were mainly accumulated in the roots of S. matsudana cuttings. With the increase in N and P concentrations, the amount of Cu and Zn that accumulates in the root of S. matsudana cuttings decreased significantly. Accumulation of Zn in the root of S. matsudana cuttings increased when translocation factors(TF) and the transport of Zn to the shoot decreased as a result of Cu treatment. Using a combination of N and P treatments(N0 + P0, N1.5 + P0.18 and N15 + P1.8, the same below),the TF of Zn under Zn50 + Cu50 treatments significantly decreased by 62.8%, 57.0%, and 77.9%, respectively,(P < 0.05)compared with that with Zn50 only. However, the accumulation of Cu in the root of S. matsudana cuttings reduced while TF and the transport of Cu to the shoot was promoted by Zn. Using the three combinations of N and P, the TF of Cu under Zn50 +Cu50 treatments significantly increased by 26.0%, 62.9%, and 42.9%(P < 0.05) compared with treatment with Cu50 only. The transport of Zn to the shoot significantly increased with the increase in N and P concentration, but the transport of Cu did not change significantly. Compared with treatment with N0 + P0 + Zn50, the TF of Zn increased by 45.6% and 247.3%(P < 0.05)under N1.5 + P0.18 + Zn50 and N15 + P1.8 + Zn50 treatment conditions, respectively. In summary, S. matsudana has a strong ability to accumulate Cu and Zn. With the increase in N and P concentration, the toxicity of heavy metals on S. matsudana could be alleviated, and the accumulation of Cu and Zn in the root decreased as the transport of Zn to shoot increased.
The effect of heavy metal pollution on growth characteristics, physiological indexes, and heavy metal accumulation was explored under eutrophication conditions using hydroponically growing Salix matsudana cuttings. The results showed that under the 50 μmol/L Cu treatment condition, cutting growth was significantly inhibited and the physiological response to stunted growth was induced, with decreasing dry weight, RGR, tolerance index(TI), and amount of photosynthetic pigment,as well as increasing MDA content and POD activity. The damage, as a result of 50 μmol/L Cu treatment in S. matsudana was more serious than that with 50 μmol/L Zn treatment. With the increase in N and P concentration, biomass increased while MDA content and POD activity decreased. Eutrophication could alleviate the damage caused by heavy metals on S. matsudana.Cu and Zn were mainly accumulated in the roots of S. matsudana cuttings. With the increase in N and P concentrations, the amount of Cu and Zn that accumulates in the root of S. matsudana cuttings decreased significantly. Accumulation of Zn in the root of S. matsudana cuttings increased when translocation factors(TF) and the transport of Zn to the shoot decreased as a result of Cu treatment. Using a combination of N and P treatments(N0 + P0, N1.5 + P0.18 and N15 + P1.8, the same below),the TF of Zn under Zn50 + Cu50 treatments significantly decreased by 62.8%, 57.0%, and 77.9%, respectively,(P < 0.05)compared with that with Zn50 only. However, the accumulation of Cu in the root of S. matsudana cuttings reduced while TF and the transport of Cu to the shoot was promoted by Zn. Using the three combinations of N and P, the TF of Cu under Zn50 +Cu50 treatments significantly increased by 26.0%, 62.9%, and 42.9%(P < 0.05) compared with treatment with Cu50 only. The transport of Zn to the shoot significantly increased with the increase in N and P concentration, but the transport of Cu did not change significantly. Compared with treatment with N0 + P0 + Zn50, the TF of Zn increased by 45.6% and 247.3%(P < 0.05)under N1.5 + P0.18 + Zn50 and N15 + P1.8 + Zn50 treatment conditions, respectively. In summary, S. matsudana has a strong ability to accumulate Cu and Zn. With the increase in N and P concentration, the toxicity of heavy metals on S. matsudana could be alleviated, and the accumulation of Cu and Zn in the root decreased as the transport of Zn to shoot increased.
引文
1郭迎庆.城市景观水体的污染控制和修复技术[J].环境科学与技术,2005,28(S1):148-150[Guo YQ.Pollution control and remediation technology for urban landscapewaters[J].Environ Sci Technol,2005,28(S1):148-150]
2李晶,栾亚宁,孙向阳,于海心,祁娜,武轩韵.水生植物修复重金属污染水体研究进展[J].世界林业研究,2015,28(2):31-35[Li J,Luan YN,Sun XY,Yu HX,Qi N,Wu XY.Research advances in remediation of heavy metal contaminated water bodies by aquatic plants[J].World For Res,2015,28(2):31-35]
3汪红,金继运.植物对锌吸收运输及积累的生理与分子机制[J].植物营养与肥料学报,2009,15(1):225-235[Wang H,Jin JY.The physiological and molecular mechanisms of zinc uptake,transport,and hyperaccumulation in plants:a review.Plant Nutr Fertili Sci,2009,15(1):225-235]
4 Tian R N,Yu S,Wang SG.Ger mination and seedling g row th of Triarrhena sacchariflora(Maxim.)Nakai under copper and cadmium stress.Ecol Environ,2011,20(8):1332-1337
5朱小龙.河蚬对富营养水体水质改善作用及生态学意义[D].无锡:江南大学,2015:7-8[Zhu XL.Corbicula fluminea improve eutrophic water quality and ecological significance[D].Wuxi:Jiangnan University,2015:7-8]
6谷照虎.水生美人蕉吸收利用硝酸盐的生理分子机制研究[D].昆明:昆明理工大学,2016:6-7[Gu ZH.The physiological and molecular mechanism of nitrate uptake and utilization in Cana generalis Bailey[D].Kunming:Kunming University of Science and Technology,2016:6-7]
7王美杰.水体富营养化的危害及防治措施[J].科技信息,2012(10):60[Wang MJ.The harm and prevention measures of water eutrophication[J].Sci Technol Inform,2012(10):60]
8胡婧,张敏.重金属污染水体修复技术的研究进展[J].轻工科技,2012(2):78-79[Hu J,Zhang M.Research progress in remediation technology of heavy metal contaminated water[J].Light Indust Sci Technol,2012(2):78-79]
9 USP Agency.Introduction to Phytoremediation[M].Boston:United States Environmental Protection Agency,2000
10 Sud D,Mahajan G,Kaur MP.Agricultural waste material as potential adsorbent for sequestering heavy metal ions from aqueous solutions:a review[J].Bioresour Technol,2008,99(14):6017-6027
11 Holm B,Heinsoo K.Municipal wastewater application to short rotation coppice of willows-treatment efficiency and clone response in Estonian case study[J].Biomass Bioenerg,2013,57:126-135
12王雯雯.柳树水培扦插对水体重金属污染修复作用研究[D].南京:南京大学,2017:103-122[Wang WW.Role of Salix hydroponic cutting in phytoremediation of water with heavy metals pollution[D].Nanjing:Nangjing University,2017:103-122]
13张富仓,康绍忠,龚道枝,李志军.不同磷浓度对玉米生长及磷、锌吸收的影响.应用生态学报,2005,16(5):903-906[Zhang FC,Kang SZ,Gong DZ,Li ZJ.Maize growth and phosphorous and zinc uptake under different phosphorous supply levels.Chin J Appl Ecol,2005,16(5):903-906]
14 Huang L,Liu C,Liu XW,Chen ZL.Immobilization of heavy metals in e-waste contaminated soils by combined application of biochar and phosphate[J].Water Air Soil Pollut,2019,230:26
15万雪琴,张帆,王长亮,丁云海.Cd、Cu、Pb处理下增施氮对巨桉生长和光合特性的影响[J].核农学报,2012,26(7):1087-1093[Wan XQ,Zhang F,Wang CL,Ding YH.Effects Of nitrogen supplement on photosynthetic characteristic and growth rate of Eucalyptus Grandis under three kind of heavy metal stress[J].J Nucl Agric Sci,2012,26(7):1087-1093]
16 Dimitriou I,Aronsson P,Weih M.Stress tolerance of five willow clones after irrigation with different amounts of landfill leachate[J].Bioresour Technol,2006,97(1):150-157
17 Mn DSU,Wieshammer G,Vega R,Wenzel WW.Hydroponic screening for metal resistance and accumulation of cadmium and zinc in twenty clones of willows and poplars[J].Environ Pollut,2007,148(1):155-165
18 Wellburn AR,Lichtenthaler H.Formulae and program to determine total carotenoids and chlorophylls A and B of leaf extracts in different solvents[J].Netherlands:Springer,1984,2:9-12
19 Rao KVM,Sresty TVS.Antioxidative parameters in the seedlings of pigeonpea(Cajanus Cajan(L.)Millspaugh)in response to Zn and Ni stresses[J].Plant Sci,2000,157:113-128
20 Herzog V,Fahimi H.Determination of the activity of peroxidase[J].Anal biochem,1973:55-62
21李俊.不同营养条件对水生植物吸收重金属影响的研究[D].长沙:中南林业科技大学,2008:4[Li J.Research on the obsorption of heavy metal by aquatic plants in different nutritions[D].Changsha:Central South University of Forestry and Technology,2008:4]
22周疆丽.蜥蜴柳对重金属的耐性研究[D].合肥:安徽农业大学,2011:18-21[Zhou JL.Study on tolerance of Salix matsudana to heavy metals[D].Hefei:Anhui Agricultural University,2011:18-21]
23高扬,辛树权,何锦冰,侯伟.铜对大蒜根尖细胞有丝分裂影响的研究[J].北方园艺,2008(6):12-14[Gao Y,Xin SQ,He JB,Hou W.The study of the effect of copper on the caryomitosis of Garlic root tips[J].North Horticult,2008(6):12-14]
24张莹,张玲,刘泓,施翔,王树凤.柳树6个无性系在铜尾矿砂中的生长及耐受性差异[J].林业科学研究,2017,30(6):936-945[Zhang Y,Zhang L,Liu H,Shi X,Wang SF.Variations in growth and tolerance of six willow clones in copper tailings soils[J].For Res,2017,30(6):936-945]
25李慧,丁刚,辛美丽,刘玮,马增岭,李大鹏,郭文.不同氮、磷浓度及配比对铜藻(Sargassum horneri)幼苗生长的影响[J].海洋与湖沼,2017,48(2):368-372[Li H,Ding G,Xin ML,Liu W,Ma ZL,Li DP,Guo W.Effects of nitrogen and phosphorus concentrations and ratios on growth of Sargassum horneri seedlings[J].Oceanol Limnol Sin,2017,48(2):368-372]
26 Kupper H,Kiipper F,Spiller M.Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants[J].JExp Bot,1996,47(295):259-266
27 Azzarello E,Pandolfi C,Giordano C,Rossi M,Mugnai S,Mancuso S.Ultramorphological and physiological modifications induced by high zinc levels in Paulownia tomentosa[J].Environ Exp Bot,2012,81(3):11-17
28李松.重金属胁迫下毛竹幼苗生理响应及其吸收规律研究[D].杭州:浙江农林大学,2015:35-39[Li S.The response of physicology and absorpation of Moso bamboo(Phyllostachys pubescens)under the heavy mental stress[D].Hangzhou:Zhejiang A&F University,2015:35-39]
29 Dunford HB,Stillman JS.On the function and mechanism of peroxidase[J].Coordin Chem Rev,1976,19:187-251
30 Luo Y,Rimmer DL.Zinc-copper interaction affecting plant growth on metalcontaminated soil[J].Environ Pollut,1995,88(1):79-83
31 Peralta-V JR,Gardea-Torresdey JL,Walton J,Mackay WP,DuarteGardea M.Effects of zinc upon tolerance and heavy metal uptake in alfalfa plants(Medicago sativa)[J].Bull Environ Contam Tox,2003,70:1036-1044
32 Bowen JE.Physiology of genotyping differences in zinc and copper uptake in rice and tomato[J].Plant Soil,1987,99:115-125
33 Sousa AI,Lilleb?AI,Pardal MA,Cacador I.Inf luence of multiple stressors on the auto-remediation processes occurring in salt marshes[J].Mar Pollut Bull,2011,62(7):1584-1587
34 Bose S,Vedamati J,Rai V,Ramanathan AL.Metal uptake and transport by Typha angustata L.grown on metal contaminated waste amended soil:an implication of phytoremediation[J].Geoderma,2008,145(1):136-142
35 Seshadri B,Bolan NS,Choppala G,Kunhikrishnan A,Sanderson P,Wang H,Currie LD,Tsang DCW,Ok YS,Kim G.Potential value of phosphate compounds in enhancing immobilization and reducing bioavailability of mixed heavy metal contaminants in shooting range soil[J].Chemosphere,2017,184:197-206
36 Bacon JR,Davidson CM.Is there a future for sequential chemical extraction?[J].Analyst,2007,133(1):25-46
37 Li SX,Lin LX,Zheng FY,Wang QX.Metal bioavailability and risk assessment from edible brown alga Laminaria japonica,using biomimetic digestion and absorption system and determination by ICP-MS[J].J Agr Food Chem,2011,59(3):822-828
38 Wallace WG,Lee BG,Luoma SN.Subcellular compartmentalization of Cd and Zn in two bivalves.I.Significance of metal-sensitive fractions(MSF)and biologically detoxified metal(BDM)[J].Mar Ecol Prog,2003,249(1):183-197
2李晶,栾亚宁,孙向阳,于海心,祁娜,武轩韵.水生植物修复重金属污染水体研究进展[J].世界林业研究,2015,28(2):31-35[Li J,Luan YN,Sun XY,Yu HX,Qi N,Wu XY.Research advances in remediation of heavy metal contaminated water bodies by aquatic plants[J].World For Res,2015,28(2):31-35]
3汪红,金继运.植物对锌吸收运输及积累的生理与分子机制[J].植物营养与肥料学报,2009,15(1):225-235[Wang H,Jin JY.The physiological and molecular mechanisms of zinc uptake,transport,and hyperaccumulation in plants:a review.Plant Nutr Fertili Sci,2009,15(1):225-235]
4 Tian R N,Yu S,Wang SG.Ger mination and seedling g row th of Triarrhena sacchariflora(Maxim.)Nakai under copper and cadmium stress.Ecol Environ,2011,20(8):1332-1337
5朱小龙.河蚬对富营养水体水质改善作用及生态学意义[D].无锡:江南大学,2015:7-8[Zhu XL.Corbicula fluminea improve eutrophic water quality and ecological significance[D].Wuxi:Jiangnan University,2015:7-8]
6谷照虎.水生美人蕉吸收利用硝酸盐的生理分子机制研究[D].昆明:昆明理工大学,2016:6-7[Gu ZH.The physiological and molecular mechanism of nitrate uptake and utilization in Cana generalis Bailey[D].Kunming:Kunming University of Science and Technology,2016:6-7]
7王美杰.水体富营养化的危害及防治措施[J].科技信息,2012(10):60[Wang MJ.The harm and prevention measures of water eutrophication[J].Sci Technol Inform,2012(10):60]
8胡婧,张敏.重金属污染水体修复技术的研究进展[J].轻工科技,2012(2):78-79[Hu J,Zhang M.Research progress in remediation technology of heavy metal contaminated water[J].Light Indust Sci Technol,2012(2):78-79]
9 USP Agency.Introduction to Phytoremediation[M].Boston:United States Environmental Protection Agency,2000
10 Sud D,Mahajan G,Kaur MP.Agricultural waste material as potential adsorbent for sequestering heavy metal ions from aqueous solutions:a review[J].Bioresour Technol,2008,99(14):6017-6027
11 Holm B,Heinsoo K.Municipal wastewater application to short rotation coppice of willows-treatment efficiency and clone response in Estonian case study[J].Biomass Bioenerg,2013,57:126-135
12王雯雯.柳树水培扦插对水体重金属污染修复作用研究[D].南京:南京大学,2017:103-122[Wang WW.Role of Salix hydroponic cutting in phytoremediation of water with heavy metals pollution[D].Nanjing:Nangjing University,2017:103-122]
13张富仓,康绍忠,龚道枝,李志军.不同磷浓度对玉米生长及磷、锌吸收的影响.应用生态学报,2005,16(5):903-906[Zhang FC,Kang SZ,Gong DZ,Li ZJ.Maize growth and phosphorous and zinc uptake under different phosphorous supply levels.Chin J Appl Ecol,2005,16(5):903-906]
14 Huang L,Liu C,Liu XW,Chen ZL.Immobilization of heavy metals in e-waste contaminated soils by combined application of biochar and phosphate[J].Water Air Soil Pollut,2019,230:26
15万雪琴,张帆,王长亮,丁云海.Cd、Cu、Pb处理下增施氮对巨桉生长和光合特性的影响[J].核农学报,2012,26(7):1087-1093[Wan XQ,Zhang F,Wang CL,Ding YH.Effects Of nitrogen supplement on photosynthetic characteristic and growth rate of Eucalyptus Grandis under three kind of heavy metal stress[J].J Nucl Agric Sci,2012,26(7):1087-1093]
16 Dimitriou I,Aronsson P,Weih M.Stress tolerance of five willow clones after irrigation with different amounts of landfill leachate[J].Bioresour Technol,2006,97(1):150-157
17 Mn DSU,Wieshammer G,Vega R,Wenzel WW.Hydroponic screening for metal resistance and accumulation of cadmium and zinc in twenty clones of willows and poplars[J].Environ Pollut,2007,148(1):155-165
18 Wellburn AR,Lichtenthaler H.Formulae and program to determine total carotenoids and chlorophylls A and B of leaf extracts in different solvents[J].Netherlands:Springer,1984,2:9-12
19 Rao KVM,Sresty TVS.Antioxidative parameters in the seedlings of pigeonpea(Cajanus Cajan(L.)Millspaugh)in response to Zn and Ni stresses[J].Plant Sci,2000,157:113-128
20 Herzog V,Fahimi H.Determination of the activity of peroxidase[J].Anal biochem,1973:55-62
21李俊.不同营养条件对水生植物吸收重金属影响的研究[D].长沙:中南林业科技大学,2008:4[Li J.Research on the obsorption of heavy metal by aquatic plants in different nutritions[D].Changsha:Central South University of Forestry and Technology,2008:4]
22周疆丽.蜥蜴柳对重金属的耐性研究[D].合肥:安徽农业大学,2011:18-21[Zhou JL.Study on tolerance of Salix matsudana to heavy metals[D].Hefei:Anhui Agricultural University,2011:18-21]
23高扬,辛树权,何锦冰,侯伟.铜对大蒜根尖细胞有丝分裂影响的研究[J].北方园艺,2008(6):12-14[Gao Y,Xin SQ,He JB,Hou W.The study of the effect of copper on the caryomitosis of Garlic root tips[J].North Horticult,2008(6):12-14]
24张莹,张玲,刘泓,施翔,王树凤.柳树6个无性系在铜尾矿砂中的生长及耐受性差异[J].林业科学研究,2017,30(6):936-945[Zhang Y,Zhang L,Liu H,Shi X,Wang SF.Variations in growth and tolerance of six willow clones in copper tailings soils[J].For Res,2017,30(6):936-945]
25李慧,丁刚,辛美丽,刘玮,马增岭,李大鹏,郭文.不同氮、磷浓度及配比对铜藻(Sargassum horneri)幼苗生长的影响[J].海洋与湖沼,2017,48(2):368-372[Li H,Ding G,Xin ML,Liu W,Ma ZL,Li DP,Guo W.Effects of nitrogen and phosphorus concentrations and ratios on growth of Sargassum horneri seedlings[J].Oceanol Limnol Sin,2017,48(2):368-372]
26 Kupper H,Kiipper F,Spiller M.Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants[J].JExp Bot,1996,47(295):259-266
27 Azzarello E,Pandolfi C,Giordano C,Rossi M,Mugnai S,Mancuso S.Ultramorphological and physiological modifications induced by high zinc levels in Paulownia tomentosa[J].Environ Exp Bot,2012,81(3):11-17
28李松.重金属胁迫下毛竹幼苗生理响应及其吸收规律研究[D].杭州:浙江农林大学,2015:35-39[Li S.The response of physicology and absorpation of Moso bamboo(Phyllostachys pubescens)under the heavy mental stress[D].Hangzhou:Zhejiang A&F University,2015:35-39]
29 Dunford HB,Stillman JS.On the function and mechanism of peroxidase[J].Coordin Chem Rev,1976,19:187-251
30 Luo Y,Rimmer DL.Zinc-copper interaction affecting plant growth on metalcontaminated soil[J].Environ Pollut,1995,88(1):79-83
31 Peralta-V JR,Gardea-Torresdey JL,Walton J,Mackay WP,DuarteGardea M.Effects of zinc upon tolerance and heavy metal uptake in alfalfa plants(Medicago sativa)[J].Bull Environ Contam Tox,2003,70:1036-1044
32 Bowen JE.Physiology of genotyping differences in zinc and copper uptake in rice and tomato[J].Plant Soil,1987,99:115-125
33 Sousa AI,Lilleb?AI,Pardal MA,Cacador I.Inf luence of multiple stressors on the auto-remediation processes occurring in salt marshes[J].Mar Pollut Bull,2011,62(7):1584-1587
34 Bose S,Vedamati J,Rai V,Ramanathan AL.Metal uptake and transport by Typha angustata L.grown on metal contaminated waste amended soil:an implication of phytoremediation[J].Geoderma,2008,145(1):136-142
35 Seshadri B,Bolan NS,Choppala G,Kunhikrishnan A,Sanderson P,Wang H,Currie LD,Tsang DCW,Ok YS,Kim G.Potential value of phosphate compounds in enhancing immobilization and reducing bioavailability of mixed heavy metal contaminants in shooting range soil[J].Chemosphere,2017,184:197-206
36 Bacon JR,Davidson CM.Is there a future for sequential chemical extraction?[J].Analyst,2007,133(1):25-46
37 Li SX,Lin LX,Zheng FY,Wang QX.Metal bioavailability and risk assessment from edible brown alga Laminaria japonica,using biomimetic digestion and absorption system and determination by ICP-MS[J].J Agr Food Chem,2011,59(3):822-828
38 Wallace WG,Lee BG,Luoma SN.Subcellular compartmentalization of Cd and Zn in two bivalves.I.Significance of metal-sensitive fractions(MSF)and biologically detoxified metal(BDM)[J].Mar Ecol Prog,2003,249(1):183-197