Arsenic hyperaccumulation by aquatic macrophytes in the Taupo Volcanic Zone, New Zealand新西兰陶波火山带大型水生植物对砷的超富集

Environmental and Experimental Botany 58 (2006) 206–215

Brett Robinson ^a,d,∗, Nick Kim ^b, Monica Marchetti ^d, Christophe Moni ^d, Lina Schroeter ^d, Carlo van den Dijssel ^d, Georgie Milne ^c, Brent Clothier ^d

a Institut f¨ur Terrestrische ¨Okologie, Universit¨atstrasse 16, ETH Zentrum CHN F24,

CH-8092 Z¨urich, Switzerland

^b Environment Waikato, P.O. Box 4010, Hamilton, New Zealand

^c Institute of Natural Resources, Massey University, Palmerston North, New Zealand

^d Hort Research, Private Bag 11 030, Palmerston North, New Zealand

Received 26 April 2005; received in revised form 27 July 2005; accepted 30 August 2005

Abstract摘要

Geothermal activity in the Taupo Volcanic Zone (TVZ), New Zealand, has resulted in elevated (0.01–0.1 mg L⁻¹) levels of arsenic (As) in many of the region’s soils, lakes and rivers. Some aquatic plants in the TVZ are known to accumulate inordinate amounts of As. We sampled 28 species of aquatic macrophytes and 11 terrestrial species from the TVZ along with ambient waters, sediments and soils. Selected aquatic species were grown in controlled conditions to examine As-uptake, tolerance, translocation and depuration. The geometric mean As concentration in 184 aquatic macrophytes was 125 mg kg⁻¹ dry weight, while the geometric mean As concentration of the 36 terrestrial samples was <0.5 mg kg⁻¹ in the above-ground portions. Some aquatic species had >1000 mg kg⁻¹ As, the threshold for As hyperaccumulation. The average As concentrations in the aquatic sediments and waters were 38 mg kg⁻¹ and 0.021 mg L⁻¹. We found a strong and positive correlation between Fe and As, along with a geometric mean Fe concentration of 3798 mg kg⁻¹. Aquatic macrophytes accumulated less As under controlled conditions compared to plants collected in situ. Arsenic was not translocated from the submerged to emergent portions of watercress. High-As specimens rapidly released As when placed in water containing <0.01 mg L⁻¹ As. Our results are consistent with the hypothesis that As accumulation by aquatic plants occurs via physicochemical adsorption to the plant’s surface, facilitated by co-deposition of other adsorptive species such as hydrated Fe oxides. Accumulation appears independent of any specific As-uptake mechanism. The aquatic plants Rorippa nasturtium-aquaticum (L.) and Mentha spp. are foraged as vegetables in the TVZ. In these species, we found respective As concentrations of up to 138 and 88 mg kg⁻¹ on a fresh weight basis. Consumption aquatic plants taken from waters with geothermal inflows may present a human health risk.

新西兰陶波火山带（TVZ）的地热活动导致该区域许多土壤、湖泊和河流中砷（As）含量升高（0.01–0.1 mg L⁻¹）。已知TVZ的一些水生植物可积累极高量的As。本研究在TVZ采集了28种大型水生植物和11种陆生植物，同时采集了相应的环境水体、沉积物和土壤样品。选取部分水生植物在受控条件下培养，以考察其对As的吸收、耐受、转运及排出。184份大型水生植物样品的As浓度几何均值为125 mg kg⁻¹（干重），而36份陆生植物样品地上部分的As浓度几何均值<0.5 mg kg⁻¹。部分水生植物As含量>1000 mg kg⁻¹，即As超富集的阈值。水生沉积物和水体中As的平均浓度分别为38 mg kg⁻¹和0.021 mg L⁻¹。Fe与As之间呈显著正相关，Fe浓度几何均值为3798 mg kg⁻¹。与原位采集的植物相比，受控条件下的大型水生植物积累的As较少。豆瓣菜中的砷未从沉水部分转运至挺水部分。将高As样品置于As浓度<0.01 mg L⁻¹的水中时，其迅速释放As。研究结果支持如下假说：水生植物对As的积累是通过植物表面的物理化学吸附实现的，并由水合铁氧化物等其他吸附性物质的共沉积所促进。该积累过程似乎不依赖于任何特定的As吸收机制。水生植物Rorippa nasturtium-aquaticum（L.）（豆瓣菜）和Mentha spp.（薄荷属）在TVZ被作为蔬菜采食。在这些植物中，以鲜重计As浓度分别高达138和88 mg kg⁻¹。食用采自有地热水汇入水体的水生植物可能对人体健康构成风险。

© 2005 Elsevier B.V. All rights reserved.

© 2005 Elsevier B.V. 版权所有。

Keywords: Arsenic; Hyperaccumulation; Aquatic macrophytes; Human health; Bioindication; Phytoremediation

关键词：砷；超富集；大型水生植物；人体健康；生物指示；植物修复

1Introduction引言

The Taupo Volcanic Zone (TVZ) covers an area of 600,000 ha in the central North Island of New Zealand. It extends from the Bay of Plenty in the north, southwest to Mount Ruapehu in a long narrow belt. The area features four active volcanoes that include Mt. Tarawera,

陶波火山带（TVZ）位于新西兰北岛中部，面积达600,000 ha。该区域呈狭长带状，北起丰盛湾，向西南延伸至鲁阿佩胡山。区内有四座活火山，包括塔拉威拉山、

^∗ Corresponding author. Tel.: +41 44 633 6073; fax: +41 44 633 1123. E-mail address: Brett.Robinson@env.ethz.ch (B. Robinson).

Mt. Tongariro, Mt. Ngauruhoe and Mt. Ruapehu. The area has widespread hydrothermal activity, and an abundance of hot springs, geysers and mud pools. The TVZ contains over 32 natural lakes, including Lake Taupo, the largest lake in New Zealand, and Lake Rotorua. New Zealand’s longest river, the Waikato, flows out of Lake Taupo, through several geothermal fields and northwestward to the Tasman Sea. Seven hydroelectric power dams have been built along this river to exploit the 366 m fall to the sea (Liddle, 1982).

汤加里罗山、瑙鲁霍伊山和鲁阿佩胡山。该区域热液活动广泛，温泉、间歇泉和泥浆池众多。TVZ内有32个以上的天然湖泊，包括新西兰最大的湖泊陶波湖以及罗托鲁阿湖。新西兰最长的河流怀卡托河发源于陶波湖，流经数个地热田后向西北注入塔斯曼海。为利用其入海前366 m的落差，沿河已建成7座水电站大坝（Liddle, 1982）。

0098-8472/$ – see front matter © 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.envexpbot.2005.08.004

0098-8472/$ – 见前页 © 2005 Elsevier B.V. 版权所有。doi:10.1016/j.envexpbot.2005.08.004

Geothermal activity in the TVZ has resulted in elevated arsenic (As) concentrations in some lakes and rivers (Aggett and Aspell, 1978). The As loading in surface waters is exacerbated by the commercial exploitation of geothermal bores for electricity (Axtmann, 1975). The condensate has elevated As concentrations. Historically, As has also been introduced into the aquatic environment from runoff of As-based pesticides (Hill, 1975), aquatic pesticides used to control lake weed (Tanner and Clayton, 1990) and leaching from timber treatment sites that used copper-chromium-arsenic (CCA) biocides.

TVZ的地热活动导致部分湖泊和河流中砷（As）浓度升高（Aggett and Aspell, 1978）。地热井用于商业发电进一步加剧了地表水的As负荷（Axtmann, 1975），其冷凝水中As浓度较高。历史上，As还通过以下途径进入水环境：含As农药的径流（Hill, 1975）、用于控制湖泊水草的水生除草剂（Tanner and Clayton, 1990），以及使用铜铬砷（CCA）杀菌剂的木材防腐处理场地的淋溶。

ThepredominantformofAsintheenvironmentisarsenate [As(V)] since arsenite [As(III)] is oxidised by atmospheric oxygen (Pepper et al., 1987). For most of the year, over 90% of the As in the Waikato River, which flows through the TVZ, is present as As(V) (Aggett and Aspell, 1978), but in the summer months the levels of As(III) increase, probably because of microbial reduction (Freeman, 1985).

环境中As的主要存在形态为砷酸盐［As(V)］，因为亚砷酸盐［As(III)］会被大气中的氧气氧化（Pepper et al., 1987）。在一年中的大部分时间里，流经TVZ的怀卡托河中90%以上的As以As(V)形态存在（Aggett and Aspell, 1978），但在夏季As(III)含量升高，这可能是微生物还原作用所致（Freeman, 1985）。

Some aquatic macrophytes growing in the TVZ and Waikato River contain high concentrations of As (Reay, 1972; Liddle, 1982). Robinson et al. (1995a) reported >1000 mg kg⁻¹ (ppm) As (dry weight) in samples of Egeria densa and Ceratophyllum demersum growing in the Waikato River system.

生长于TVZ和怀卡托河中的一些大型水生植物含有高浓度的As（Reay, 1972; Liddle, 1982）。Robinson et al.（1995a）报道，怀卡托河水系中生长的Egeria densa和Ceratophyllum demersum样品中As含量>1000 mg kg⁻¹（ppm）（干重）。

A survey of watercress (Rorippa nasturtium-aquaticum) growing in the region revealed concentrations as high as 1766 mg kg⁻¹ As (dry weight) in the shoots (Robinson et al., 2003). On a fresh weight basis, the average leaf As concentration was 29 mg kg⁻¹. This is of concern to human health, because foraged watercress is consumed as a vegetable. Plant accumulation of As may also facilitate its entry into the food chain.

对该地区生长的豆瓣菜（Rorippa nasturtium-aquaticum）的调查表明，其地上部As浓度高达1766 mg kg⁻¹（干重）（Robinson et al., 2003）。以鲜重计，叶片As平均浓度为29 mg kg⁻¹。由于野外采摘的豆瓣菜被作为蔬菜食用，这对人体健康构成隐患。植物对As的积累还可能促进其进入食物链。

The effects of sub-acute As poisoning include an increased incidence of cancer, particularly of the bladder, liver and lungs (Morales et al., 2000; Storelli and Marcotrigiano, 2001). Inorganic As is considerably more toxic than organic As (FSANZ, 2002). There is currently some debate over appropriate tolerable daily intakes (TDIs) for inorganic As, as older numbers come up for review. Regulatory TDIs now range from 0.3 to 2.1 �g kg⁻¹ of body weight per day (USEPA, 1993; ATSDR, 2000; Baars et al., 2001). However, progressively more conservative values are being adopted.

亚急性As中毒的影响包括癌症发病率上升，尤其是膀胱癌、肝癌和肺癌（Morales et al., 2000; Storelli and Marcotrigiano, 2001）。无机As的毒性远高于有机As（FSANZ, 2002）。随着早期标准值陆续进入复审，目前对于无机As适宜的每日耐受摄入量（TDI）仍存在一定争议。现行法规中的TDI为每天0.3至2.1 μg kg⁻¹体重（USEPA, 1993; ATSDR, 2000; Baars et al., 2001），但所采用的数值正日趋保守。

Liddle (1982) investigated the uptake of As by C. demersum. He found that plants grown in As solutions with <0.1 mg L⁻¹ As (III or V) reached a maximum concentration in 1 or 2 days, while plants in >0.5 mg L⁻¹ As required up to a week. Arsenic concentration in plants increased with increasing concentration of As in the growing medium. At a similar As concentration in the growing medium, plants grown under laboratory conditions contained far less As than plants collected under natural conditions in the Waikato River.

Liddle（1982）研究了C. demersum对As的吸收。他发现，生长于As浓度<0.1 mg L⁻¹（III价或V价）溶液中的植物在1–2天内即达到最高浓度，而在>0.5 mg L⁻¹ As溶液中的植物则需长达一周。植物中As浓度随生长介质中As浓度的升高而增加。在生长介质As浓度相近的情况下，实验室条件下培养的植物所含As远低于怀卡托河自然条件下采集的植物。

Arsenic uptake by plants is associated with the phosphate ion (H2PO4⁻). Arsenic(V) is taken up as an H2PO4⁻ analogue (Khattak et al., 1991; Meharg and Macnair, 1991; Pickering et al., 2000). Aquatic plants have been shown to accumulate trace elements by absorption followed by passive or active transport across membranes (Forstner and Wittmann, 1981; Smies, 1983).

植物对砷的吸收与磷酸根离子（H2PO4⁻）有关。As(V)作为H2PO4⁻的类似物被吸收（Khattak et al., 1991; Meharg and Macnair, 1991; Pickering et al., 2000）。已有研究表明，水生植物通过吸收并随后经被动或主动跨膜运输来积累微量元素（Forstner and Wittmann, 1981; Smies, 1983）。

Ma et al. (2001) reported As concentrations in the Brake fern, Pteris vittata, of up to 22,000 mg kg⁻¹ (2.2%) on a dry weight basis. This is the first terrestrial species reported to take-up As to concentrations greater than 1000 mg kg⁻¹, the threshold for a plant to be considered a ‘hyperaccumulator’ (Brooks et al., 1977). Hyperaccumulator plants could be used for the phytoremediation of As-contaminated sites (Ma et al., 2001). This technology relies on plants that translocate inordinate amounts of one or more metal(loid)s, including As, into their above-ground biomass. Arsenic phytoremediation would involve the repeated cropping until the soil’s As concentration has reached an acceptable level. After each cropping, the plant biomass would be removed from the area and may be burned to reduce its volume, whereupon it could be stored in an appropriate area, such as a contained landfill that does not pose a risk to the environment. The possibility of using hyperaccumulator plants to extract As from aquatic environments has also been suggested (Brooks and Robinson, 1998).

Ma et al.（2001）报道，蜈蚣草（Pteris vittata）中As浓度以干重计高达22,000 mg kg⁻¹（2.2%）。这是首个被报道As吸收浓度超过1000 mg kg⁻¹的陆生物种，而该值正是植物被认定为“超富集植物”的阈值（Brooks et al., 1977）。超富集植物可用于As污染场地的植物修复（Ma et al., 2001）。该技术依赖于能将极高量的一种或多种金属（类金属）（包括As）转运至地上生物量的植物。砷的植物修复需反复种植收割，直至土壤As浓度降至可接受水平。每次收割后，将植物生物量移出该区域，可通过焚烧减小体积，随后贮存于适当场所，如不会对环境构成风险的封闭式填埋场。利用超富集植物从水环境中提取As的可能性也已被提出（Brooks and Robinson, 1998）。

The aim of this study was to investigate the nature and extent of As-uptake by aquatic and terrestrial plant species that occur in a high-As environment. In particular, we sought to measure As-uptake by aquatic species in both controlled conditions and in the field with a view to determining the potential implications for human health, phytoremediation and the fate of As.

本研究旨在探讨高As环境中水生和陆生植物对As吸收的性质与程度。特别是，我们试图在受控条件和野外条件下测定水生植物对As的吸收，以明确其对人体健康、植物修复以及As归趋的潜在影响。

2Materials and methods材料与方法

Aquatic plants were sampled from 11 sites along the Waikato River, and from four other waterways with geothermal inflows (Fig. 1). Whole specimens were taken and washed in river water to remove sediment. Further washing in distilled water was carried out upon returning to the laboratory. Water and sediment samples were collected from all sites and stored in sealed containers.

水生植物采自怀卡托河沿岸11个采样点以及另外4条有地热水汇入的水道（图1）。采集完整植株，并用河水冲洗以去除沉积物，返回实验室后再用蒸馏水进一步清洗。在所有采样点采集水样和沉积物样品，并贮存于密封容器中。

Leaves were collected from selected terrestrial plant species growing near geothermal springs at five locations, along with accompanying soil samples from four of the five locations (Fig. 1).

在5个地点采集了生长于地热泉附近的部分陆生植物的叶片，并在其中4个地点采集了相应的土壤样品（图1）。

2.1. Watercress and native ferns grown in soil2.1. 土壤中培养的豆瓣菜和本土蕨类植物

The greenhouse experiment was performed at HortResearch, Palmerston North, New Zealand (40.2^◦S, 175.4^◦E). Five species of native ferns (Asplenium bulbiferum, Blechnum discolor, Histiopteris incisa, Pneumatopteris penningera and Polystichum vestitum) as well as watercress (R. nasturtium-aquaticum) were grown in 15 L buckets containing soils spiked with sodium arsenate (Analytical Reagent [AR] grade) to give final concentrations of 0, 55 and 105 mg kg⁻¹. There were five replicates for each treatment.

温室试验在新西兰北帕默斯顿HortResearch进行（40.2^◦S, 175.4^◦E）。将5种本土蕨类植物（Asplenium bulbiferum、Blechnum discolor、Histiopteris incisa、Pneumatopteris penningera和Polystichum vestitum）以及豆瓣菜（R. nasturtium-aquaticum）种植于15 L桶中，桶内土壤添加砷酸钠（分析纯［AR］级），使最终浓度分别为0、55和105 mg kg⁻¹。每个处理设5个重复。

The soil used was Manawatu fine sandy loam (Dystric Fluventic Eutropchrept) (Vogeler et al., 2001), with a pH of 4.4, total organic carbon 6.3% and an exchange capacity of 13.4 cmol(+) kg⁻¹. Soils were prepared by adding varying amounts of a 1% As solution to 15 kg of soil. This was mixed using a concrete mixer. Soils were fertilised with Nitrosol^TM liquid fertiliser (N:P:K. of 8:3:6 Rural Research Limited, P.O. BOX 12773 Penrose, Auckland, New Zealand) at a rate recommended by the manufacturer. Planting occurred at the end of October 2002, some 6 weeks after preparation of the pots. This delay was to allow time for the added As to reach an equilibrium with the soil. Plants were watered according to evaporative demand. Pots were arranged in a randomised block design within a greenhouse. Plant samples were taken for analysis in mid-January, 2003, 10 weeks after planting.

供试土壤为Manawatu细砂壤土（Dystric Fluventic Eutropchrept）（Vogeler et al., 2001），pH为4.4，总有机碳6.3%，交换量为13.4 cmol(+) kg⁻¹。在15 kg土壤中加入不同量的1% As溶液，并用混凝土搅拌机混匀。按生产商推荐用量施用Nitrosol^TM液体肥料（N:P:K为8:3:6，Rural Research Limited, P.O. BOX 12773 Penrose, Auckland, New Zealand）。于2002年10月底种植，距盆土制备约6周，以使添加的As与土壤达到平衡。根据蒸散需求浇水。盆钵在温室内按随机区组设计排列。于2003年1月中旬（种植后10周）采集植物样品进行分析。

2.2. The uptake of As from spiked river water by aquatic plants

2.2. 水生植物对加砷河水中As的吸收

The As-uptake and tolerance of watercress (R. nasturtium-aquaticum), Myriophyllum propinquum and C. demersum were determined in simulated aquatic conditions by growing free-floating plants in 2 L jars filled (to 1.5 L) with As-spiked river water. Each jar was covered with clear plastic containing two small holes: one for a bubbler tube and the other to let the air escape. In addition, cuttings of watercress (R. nasturtium-aquaticum) were grown hydroponically in 250 mL Erlenmeyer flasks to elucidate its capacity to tolerate, translocate and store As. Here, the plant was suspended through a polystyrene bung, so that half of the stem and nascent roots were suspended in solution, while the aerial stems and leaves remained isolated from any As solution.

在模拟水生条件下，将豆瓣菜（R. nasturtium-aquaticum）、Myriophyllum propinquum和C. demersum以自由漂浮方式培养于2 L广口瓶中（装入1.5 L加砷河水），以测定其对As的吸收与耐受。每个瓶口覆盖透明塑料膜，膜上开两个小孔：一个用于插入通气管，另一个用于排气。此外，将豆瓣菜（R. nasturtium-aquaticum）插条置于250 mL锥形瓶中水培，以阐明其对As的耐受、转运和贮存能力。植株穿过聚苯乙烯塞悬挂，使一半茎和新生根浸没于溶液中，而气生茎和叶片则与As溶液隔离。

For the growth experiment, we collected watercress plants from waterways around the Manawatu Region, near the city of Palmerston North, New Zealand. This area has no known As contamination. Plants with a fresh weight of approximately 18 g were accurately weighed, and then one plant was placed into each jar or Erlenmeyer flask. The jars and flaskswerefilledwithriverwater(TuriteaStream,Palmerston North) and As added (as 1000 mg As L⁻¹ AR Na2HAsO4) to give approximate final solutions of 0.1, 0.3, 1 and 3 mg L⁻¹ As. Jars and Erlenmeyer flasks containing no added As (controls) were also prepared. Additional treatments of 10 and 30 mg L⁻¹ were prepared for watercress in the Erlenmeyer flasks. There were three replicates for each species at each concentration. The experiment was set up in May, 2003 and lasted for 6 weeks. After 3 weeks, the solutions in the Erlenmeyerflaskswerereplaced.Aliquotsof4 mLofsolutionwere taken from each container at the start of the experiment and then at 48 h intervals, to determine when the solutions had reached a quasi-equilibrium concentration. We assumed this point to have been reached when there was only a negligible change in the solution As concentration, presumably caused by plant-growth. All plants in all treatments had reached this point after 6 weeks. The plants in jars were then removed, washed thoroughly in distilled water and the fresh and dry weights determined. The dried plant material was then analysed for As.

生长试验所用豆瓣菜采自新西兰北帕默斯顿市附近Manawatu地区的水道，该区域无已知的As污染。准确称取鲜重约18 g的植株，每个广口瓶或锥形瓶中放入一株。瓶中装入河水（Turitea Stream，北帕默斯顿），并添加As（以1000 mg As L⁻¹的分析纯Na2HAsO4形式），使最终溶液浓度约为0.1、0.3、1和3 mg L⁻¹ As。同时设置未添加As的广口瓶和锥形瓶作为对照。锥形瓶中的豆瓣菜另设10和30 mg L⁻¹两个处理。每个物种每个浓度设3个重复。试验于2003年5月开始，持续6周。3周后更换锥形瓶中的溶液。试验开始时及此后每隔48 h从各容器中取4 mL溶液，以确定溶液何时达到准平衡浓度。当溶液As浓度变化可忽略（推测由植物生长引起）时，即认为已达到该状态。6周后所有处理的全部植株均达到该状态。随后将广口瓶中的植株取出，用蒸馏水彻底清洗，测定鲜重和干重，并分析干燥植物材料中的As。

The aerial portions of watercress grown in flasks were excised, washed in distilled water, the stems and leaves separated and the fresh and dry weights determined. The submerged portions were washed in distilled water, the roots and stems separated and the fresh and dry weights determined.

将锥形瓶中培养的豆瓣菜地上部分剪下，用蒸馏水清洗，分离茎和叶，并测定鲜重和干重。沉水部分用蒸馏水清洗后分离根和茎，测定鲜重和干重。

The volume of the ambient solution in the jars was measured at the end of the experiment. On average, 110 mL (7%) of solution had evaporated from each jar. Here, we report the final solution concentrations. Evapotranspiration from the Erlenmeyer flasks was not determined. The reported concentrations therefore represent initial values.

试验结束时测定广口瓶中环境溶液的体积，平均每瓶蒸发了110 mL（7%）溶液。本文报告的是最终溶液浓度。锥形瓶的蒸散量未测定，因此所报告的浓度为初始值。

2.3. Arsenic depuration by aquatic plants2.3. 水生植物的砷排出

An experiment was set up to determine the retention of As by aquatic plants when placed in an ambient solution containing negligible amounts of As. Live specimens of watercress (R. nasturtium-aquaticum) and M. propinquum were collected from Tokaanu hot springs at the Southern end of Lake Taupo. The ambient water concentration was 0.18 mg L⁻¹ As. Upon returning to the laboratory, 18 g portions of fresh material were placed in jars containing 1.5 L of Turitea River water with an As concentration of less than 0.01 mg L⁻¹. There were five replicates of R. nasturtium-aquaticum and three of M. propinquum. Water samples (5 mL aliquots) were taken regularly for 25 days. At the end of the experiment, the plants and waters were treated the same as those in the As-uptake experiment described above. The initial As concentrations of the plants tested were calculated at the end of the experiment by adding the amount of As remaining in the plant to that contained in the ambient water and dividing the sum by the final dry biomass of the plant. This calculation assumes that there was negligible growth during the experiment. The calculated initial As concentrations were compared to 18 other specimens of R. nasturtium-aquaticum and 10 other specimens of M. propinquum that were collected from the same site.

设置试验以测定水生植物置于As含量可忽略的环境溶液中时对As的保持情况。从陶波湖南端的Tokaanu温泉采集豆瓣菜（R. nasturtium-aquaticum）和M. propinquum的活体样品，其环境水体As浓度为0.18 mg L⁻¹。返回实验室后，将18 g鲜样置于装有1.5 L Turitea河水（As浓度低于0.01 mg L⁻¹）的广口瓶中。R. nasturtium-aquaticum设5个重复，M. propinquum设3个重复。在25天内定期采集水样（每次5 mL）。试验结束时，植物和水样的处理方法与上述As吸收试验相同。供试植物的初始As浓度在试验结束时计算得出：将植物中残留的As量与环境水体中的As量相加，再除以植物最终干生物量。该计算假设试验期间植物生长可忽略。将计算得到的初始As浓度与同一地点采集的另外18个R. nasturtium-aquaticum样品和10个M. propinquum样品进行比较。

2.4. Sample preparation and As determination2.4. 样品制备与As测定

Plant material and soils were placed in a drying cabinet at 80 ^◦C until a constant weight was reached. Plant material was ground using a mortar and pestle. Soil samples were sieved to <1 mm size using a nylon sieve and stored in sealed plastic bags.

将植物材料和土壤置于80 ^◦C烘箱中烘至恒重。植物材料用研钵研磨。土壤样品用尼龙筛过<1 mm筛，并贮存于密封塑料袋中。

Between 0.15 and 0.2 g of ground plant material, or 0.5 g of sieved soil or sediment sample, were accurately weighed into 50 mL Erlenmeyer flasks. Ten mL of concentrated nitric acid (69%) were added to each flask and the mixturesheatedandevaporatedonaheatingblockuntilafinal volume of about 3 mL was reached. The samples were then diluted to 10 mL using distilled water and stored in polythene containers.

准确称取0.15–0.2 g磨碎的植物材料，或0.5 g过筛的土壤或沉积物样品，置于50 mL锥形瓶中。每瓶加入10 mL浓硝酸（69%），在加热板上加热蒸发至最终体积约3 mL。随后用蒸馏水稀释至10 mL，贮存于聚乙烯容器中。

All samples of plant material, soils and waters were analysed for As using graphite-furnace, atomic-absorption spectroscopy. Due to the high concentrations of As measured in some plant samples, plant standards were unavailable. Thus, for quality assurance, 15 dried and ground aquatic plant samples from the TVZ were sent to a commercial laboratory (Hill Laboratories, Hamilton, New Zealand) for the determination of As and other elements by inductively coupled plasma mass spectroscopy (ICPMS). The species analysed (with the site no. shown in Fig. 1) were: Agrostis sp. (12), Ceratophyllum demersum (4,4,6,7,8), E. densa (10), Elodea canadensis (12), Juncus sp. (1), Lagarosiphon major (11), Mentha spicata (12), M. propinquum (12,12), Polygonum salicifolium (12) and R. nasturtium-aquaticum (12). Our results were in good agreement (R² = 0.978) with those of the commercial laboratory.

所有植物、土壤和水样均采用石墨炉原子吸收光谱法测定As。由于部分植物样品As浓度很高，无可用的植物标准物质。因此，为进行质量保证，将15份来自TVZ的干燥磨碎水生植物样品送至商业实验室（Hill Laboratories，新西兰汉密尔顿），采用电感耦合等离子体质谱法（ICPMS）测定As及其他元素。所分析的物种（括号内为图1中的采样点编号）为：Agrostis sp.（12）、Ceratophyllum demersum（4,4,6,7,8）、E. densa（10）、Elodea canadensis（12）、Juncus sp.（1）、Lagarosiphon major（11）、Mentha spicata（12）、M. propinquum（12,12）、Polygonum salicifolium（12）和R. nasturtium-aquaticum（12）。本研究结果与商业实验室的结果吻合良好（R² = 0.978）。

2.5. Statistical treatment of data2.5. 数据统计处理

MINITAB (Minitab Inc., Pennsylvania State University, University Park, Pennsylvania) was used for ANOVA (at the 5% level) and correlation analyses. Data that were log-normally distributed were log-transformed for statistical analyses. For log-normal data, we report geometric means and standard deviation ranges rather than means and standard deviations. With log-normal data, the geometric mean is a better measure of central tendency than the arithmetic mean. Use of geometric means reduces distortions caused by a few anomalous values and produces a value of better centrality.

采用MINITAB（Minitab Inc., Pennsylvania State University, University Park, Pennsylvania）进行ANOVA（5%显著性水平）和相关性分析。呈对数正态分布的数据经对数转换后进行统计分析。对于对数正态数据，报告几何均值和标准差范围，而非算术均值和标准差。对于对数正态数据，几何均值比算术均值更能反映集中趋势。采用几何均值可减少少数异常值造成的偏差，得到集中性更好的数值。

3Results结果

3.1. Arsenic accumulation in terrestrial and aquatic plants from the TVZ and Waikato River3.1. TVZ和怀卡托河陆生及水生植物中的砷积累

The average As concentrations in the waters, sediments and soils, as well as aquatic and terrestrial plants collected from the TVZ, are presented in Table 1. The geometric mean As concentration in the water samples was over twice that of the New Zealand Drinking Water Standard (0.01 mg L⁻¹). The pH of the water samples ranged between 5.9 and 6.4, with a geometric mean of 6.3 (pH data are not shown in the tables or figures).

从TVZ采集的水、沉积物、土壤以及水生和陆生植物中的As平均浓度见表1。水样As浓度的几何均值是新西兰饮用水标准（0.01 mg L⁻¹）的两倍以上。水样pH为5.9–6.4，几何均值为6.3（pH数据未在图表中列出）。

There was a clear demarcation between terrestrial plants, which accumulated negligible concentrations of As, and aquatic species that had As concentrations manifold higher than the ambient waters from where they were taken.

陆生植物与水生植物之间存在明显区别：陆生植物积累的As浓度可忽略不计，而水生植物的As浓度则比其所在环境水体高出许多倍。

A summary of As concentrations in 28 aquatic species and 11 terrestrial species from the Waikato River and TVZ is given in Tables 2 and 3, respectively. The data clearly display the difference in As accumulation between aquatic and terrestrial plants. All aquatic plants accumulated measurable As concentrations with nine species (30%) exceeding 1000 mg kg⁻¹ on a dry weight (d.w.) basis, the threshold for hyperaccumulation (Brooks et al., 1977). By contrast, 83% of the terrestrial plants (Table 3) were below detection limits for As (<0.5 mg kg⁻¹). All the aquatic plants accumulated As to concentrations greater than 5 mg kg⁻¹. None of the terrestrial plants had As concentrations surpassing 11 mg kg⁻¹.

怀卡托河和TVZ中28种水生植物和11种陆生植物的As浓度分别汇总于表2和表3。数据清楚地显示了水生植物与陆生植物在As积累上的差异。所有水生植物均积累了可测浓度的As，其中9种（30%）以干重（d.w.）计超过1000 mg kg⁻¹，即超富集阈值（Brooks et al., 1977）。相比之下，83%的陆生植物（表3）As含量低于检出限（<0.5 mg kg⁻¹）。所有水生植物积累的As浓度均大于5 mg kg⁻¹，而陆生植物的As浓度均未超过11 mg kg⁻¹。

The bioaccumulation coefficient (B.C.) is defined here as the plant/water concentration quotient. The B.C. indicates the efficacy of plant As-accumulation. The geometric means of the bioaccumulation coefficients for the aquatic plants tested in this experiment are shown in Table 2. The results presented here show only the plant/water bioaccumulation coefficient. Some of the aquatic plants tested were rooted to sediments that had an As concentration that was many times the level of the water. An ANOVA test revealed that there was no significant difference (p = 0.25) in the As concentrations of rooted and free-floating plants.

本文将生物富集系数（B.C.）定义为植物/水体浓度之比。B.C.反映植物积累As的效率。本试验所测水生植物生物富集系数的几何均值见表2。此处仅给出植物/水体生物富集系数。部分受试水生植物扎根于沉积物中，而沉积物的As浓度是水体的许多倍。ANOVA检验表明，扎根植物与自由漂浮植物的As浓度无显著差异（p = 0.25）。

The geometric means and standard deviation ranges of the As concentrations waters (mg L⁻¹), as well as soils, sediments, aquatic and terrestrial plants (mg kg⁻¹ dry weight) from the Taupo Volcanic Zone

陶波火山带水体（mg L⁻¹）以及土壤、沉积物、水生和陆生植物（mg kg⁻¹干重）中As浓度的几何均值与标准差范围

The sampling locations are shown in Fig. 1.

采样地点见图1。

3.2. Arsenic accumulation in ferns and watercress from As-spiked soil3.2. 加砷土壤中蕨类植物和豆瓣菜的砷积累

The ferns and watercress grew well in all the treatments, and there were no signs of As toxicity. None of the fern species or the watercress had foliar As concentrations greater than 0.5 mg kg⁻¹, the detection limit for As, even at the highest soil concentration of 105 mg kg⁻¹. There were no significant differences in the soil As concentration before and after the experiment, indicating that leaching losses were minimal.

蕨类植物和豆瓣菜在所有处理中均生长良好，未表现出As毒害症状。即使在最高土壤浓度105 mg kg⁻¹下，所有蕨类植物和豆瓣菜的叶片As浓度均未超过As检出限0.5 mg kg⁻¹。试验前后土壤As浓度无显著差异，表明淋溶损失极小。

3.3. Arsenic tolerance and accumulation by aquatic plants under controlled conditions

3.3. 受控条件下水生植物对砷的耐受与积累

None of the free-floating plants in jars showed necrosis or growth distortion in any of the treatments. All three species increased in biomass (Fig. 2A). However, there was a significant negative correlation (r = −0.87, p < 0.01) between biomass production by C. demersum and the ambient As concentration. There was also a significant decrease (p = 0.02) in the growth of M. propinquum, between 0.17 and 0.29 mg L⁻¹ in the ambient solution. The growth of watercress (R. nasturtium-aquaticum) was not significantly affected. Fig. 2B shows the final As concentrations in the plants after 6 weeks of growth. In the control treatment, the As concentrations of the control plants and that of the ambient water were below the detection limits of 0.5 mg kg⁻¹ and 0.01 mg L⁻¹, respectively. This indicates that there were negligible amounts of As in the plants at the beginning of the experiment. When As was added to the ambient solution, there were significant differences (p < 0.01) between the extent of accumulation for each species: C. demersum ≫ M. propinquum > R. nasturtium-aquaticum. At the highest As levels in the ambient solution, 3.9 mg L⁻¹, the plant As concentrations were similar to those sampled from the TVZ and Waikato River. However, under these conditions, the bioaccumulation coefficients (Fig. 2C) for all three species were 1–2 orders of magnitude lower than the plants collected in situ.

广口瓶中的自由漂浮植物在所有处理中均未出现坏死或生长畸形。三个物种的生物量均有所增加（图2A）。然而，C. demersum的生物量生产与环境As浓度呈显著负相关（r = −0.87，p < 0.01）。环境溶液As浓度在0.17至0.29 mg L⁻¹之间时，M. propinquum的生长也显著下降（p = 0.02）。豆瓣菜（R. nasturtium-aquaticum）的生长未受到显著影响。图2B显示了生长6周后植物中的最终As浓度。在对照处理中，对照植物和环境水体的As浓度分别低于检出限0.5 mg kg⁻¹和0.01 mg L⁻¹，表明试验开始时植物中的As含量可忽略不计。向环境溶液中添加As后，各物种的积累程度存在显著差异（p < 0.01）：C. demersum ≫ M. propinquum > R. nasturtium-aquaticum。在环境溶液最高As浓度3.9 mg L⁻¹下，植物As浓度与TVZ和怀卡托河采集的样品相近。然而，在此条件下，三个物种的生物富集系数（图2C）均比原位采集的植物低1–2个数量级。

Fig. 3A shows the As accumulation in various portions of watercress grown hydroponically in Erlenmeyer flasks. On average, the submerged roots and stems had an As concentration an order of magnitude higher than the aerial stems and leaves. The growth of watercress (Fig. 3B) was unaffected at and below 1.03 mg L⁻¹. This threshold is well above water As concentrations found in the aquatic environment of the TVZ or Waikato River. Plants grown above this concentration showed signs of stress, in particular through the disintegration of the submerged portions. At the highest concentration of 25.8 mg L⁻¹ the fresh weight decreased during the experiment, indicating that the plant was dying.图3A显示了锥形瓶中水培豆瓣菜各部位的As积累情况。沉水根和茎的As浓度平均比气生茎和叶高一个数量级。在1.03 mg L⁻¹及以下浓度，豆瓣菜的生长（图3B）未受影响。该阈值远高于TVZ或怀卡托河水环境中的水体As浓度。在高于此浓度下生长的植株表现出胁迫症状，尤其是沉水部分发生解体。在最高浓度25.8 mg L⁻¹下，试验期间植株鲜重下降，表明植株正在死亡。

3.4. Depuration of As by aquatic plants3.4. 水生植物的砷排出

When placed in uncontaminated river water at <0.01 mg L⁻¹ As, As-rich watercress (R. nasturtium-aquaticum) and M. propinquum released 62(±25)% and 21(±5)% of their total As into the ambient water. The calculated geometric means and standard deviation ranges of the initial concentrations were 2364 (1964–2485) mg kg⁻¹ As for R. nasturtium-aquaticum and 1976 (1353–2886) mg kg⁻¹ As for M. propinquum.

将富As的豆瓣菜（R. nasturtium-aquaticum）和M. propinquum置于As浓度<0.01 mg L⁻¹的未污染河水中后，二者分别向环境水体释放了其总As量的62(±25)%和21(±5)%。计算得到的初始浓度几何均值及标准差范围为：R. nasturtium-aquaticum 2364 (1964–2485) mg kg⁻¹ As，M. propinquum 1976 (1353–2886) mg kg⁻¹ As。

Arsenic accumulation in the submerged portions of aquatic species collected from the Taupo Volcanic Zone

陶波火山带采集的水生植物沉水部分的砷积累

The numbers in the “Location” column refer to sites shown in Fig. 1. “% dry weight” indicates the percentage dry matter in the fresh weight plant. Plant concentrations are in mg kg⁻¹ dry weight, water concentrations are in mg L⁻¹. The “hot water” and “cold water” algae represent an assemblage of prokaryotic and eukaryotic photosynthetic-organisms that included both single celled and filamentous species. Plus (+) denotes species that lack extensive root systems. ^a Bioaccumulation coefficient, defined here as the plant/water concentration quotient.

“Location”（地点）栏中的编号对应图1所示采样点。“% dry weight”表示鲜重植物中干物质所占百分比。植物浓度单位为mg kg⁻¹干重，水体浓度单位为mg L⁻¹。“热水”和“冷水”藻类代表由原核和真核光合生物组成的群落，包括单细胞和丝状物种。加号（+）表示缺乏发达根系的物种。^a 生物富集系数，此处定义为植物/水体浓度之比。

The measured concentrations from other specimens from the same site were 1390 (666–2904) mg kg⁻¹ As for R. nasturtium-aquaticum and 2102 (874–5056) mg kg⁻¹ As for M. propinquum. The final ambient solution As concentrations for R. nasturtium-aquaticum and M. propinquum were 0.42 (0.25–0.69) and 0.24 (0.16–0.37) mg L⁻¹. During this time, the plants showed no signs of necrosis and had visible growth. The change in biomass was not recorded.

同一地点其他样品的实测浓度为：R. nasturtium-aquaticum 1390 (666–2904) mg kg⁻¹ As，M. propinquum 2102 (874–5056) mg kg⁻¹ As。R. nasturtium-aquaticum和M. propinquum环境溶液的最终As浓度分别为0.42 (0.25–0.69)和0.24 (0.16–0.37) mg L⁻¹。在此期间，植株未出现坏死症状，并有明显生长。生物量变化未作记录。

Arsenic concentrations (mg kg⁻¹ dry weight) in the leaves of terrestrial species collected from the Taupo Volcanic Zone陶波火山带采集的陆生植物叶片中的砷浓度（mg kg⁻¹干重）

The numbers in the “Location” column refer to sites shown in Fig. 1. The soil concentrations for sites 11, 12, 14 and 15 were 80.2, 33.2, 36.4 and 67.9, respectively. No soil was sampled from site 13.

“Location”（地点）栏中的编号对应图1所示采样点。采样点11、12、14和15的土壤浓度分别为80.2、33.2、36.4和67.9。采样点13未采集土壤。

Watercress did not reach equilibrium even after 25 days, although over half of the final concentration in the ambient solution was reached after 5 days. There was no consistent trend for M. propinquum. However, like watercress, over half of the final concentration in the ambient solution was achieved after 5 days.

豆瓣菜即使在25天后仍未达到平衡，但在5天后环境溶液已达到最终浓度的一半以上。M. propinquum无一致的变化趋势，但与豆瓣菜类似，5天后环境溶液也已达到最终浓度的一半以上。

3.5. Accumulation of other elements by aquatic plants3.5. 水生植物对其他元素的积累

The results of the multi-element analysis are given in Table 4. In addition to As, the plants also had elevated levels of other chalcophile elements, notably Fe, Sb, Hg, Tl and Se. The Fe concentrations in the aquatic plants were significantly and positively correlated with all the chalcophilic elements, including As (r = 0.68, p < 0.01). The concentrations in Table 4 are the means of 10 aquatic species. Therefore, the results do not show any species-specific patterns that may have been present.

多元素分析结果见表4。除As外，植物中其他亲硫元素（尤其是Fe、Sb、Hg、Tl和Se）的含量也较高。水生植物中的Fe浓度与所有亲硫元素（包括As）均呈显著正相关（r = 0.68，p < 0.01）。表4中的浓度为10种水生植物的平均值，因此结果未能反映可能存在的物种特异性规律。

The geometric means, standard deviation ranges and maximum values of elemental concentrations (mg kg⁻¹ dry weight) in 15 selected aquatic plants from the Taupo Volcanic Zone, New Zealand

新西兰陶波火山带15份水生植物样品中元素浓度（mg kg⁻¹干重）的几何均值、标准差范围和最大值

4Discussion讨论

4.1. Contrasting As-uptake between aquatic and terrestrial vegetation4.1. 水生与陆生植被对As吸收的差异

All the aquatic plants in the TVZ and Waikato River had As concentrations 100–50,000 times that of the ambient water. Most specimens of M. propinquum were over the 1000 mg kg⁻¹ threshold. There have been no previous reports of As hyperaccumulation by this species.

TVZ和怀卡托河中所有水生植物的As浓度均为环境水体的100–50,000倍。M. propinquum的大多数样品超过了1000 mg kg⁻¹的阈值。此前尚无该物种超富集As的报道。

Previous studies of aquatic plants from the TVZ (Liddle, 1982; Robinson et al., 1995a, 2003; Brooks and Robinson, 1998) focused on four species: C. demersum, E. densa, Lagarosiphon major and R. nasturtium-aquaticum. These previous studies reported average As concentrations in C. demersum, E. densa, L. major and R. nasturtium, of 400, 500, 300 and 400 mg kg⁻¹, respectively. Although sampled at different locations, our results were in good agreement.

以往对TVZ水生植物的研究（Liddle, 1982; Robinson et al., 1995a, 2003; Brooks and Robinson, 1998）集中于4个物种：C. demersum、E. densa、Lagarosiphon major和R. nasturtium-aquaticum。这些研究报道的C. demersum、E. densa、L. major和R. nasturtium中As平均浓度分别为400、500、300和400 mg kg⁻¹。尽管采样地点不同，本研究结果与之吻合良好。

Meanwhile,Aswasnottakenuptoanyextentbyterrestrial vegetation. Outridge and Noller (1991) reported a difference in trace-element accumulation between aquatic and terrestrial species. In terrestrial systems, solubilisation of As in the rhizosphere is necessary to allow root uptake. An efficient As transport and storage system would be needed for leaf accumulation to occur. Neither of these need be the case when the plant grows in an aqueous medium. Here the metalloid is already present in a bioavailable form and can be absorbed or adsorbed by the leaves.

与此同时，陆生植被几乎不吸收As。Outridge and Noller（1991）报道了水生与陆生物种在微量元素积累上的差异。在陆地系统中，As须在根际溶解后才能被根系吸收，而叶片积累As还需要高效的As转运和贮存系统。当植物生长于水介质中时，这两者均非必需，因为此时类金属已以生物有效形态存在，可被叶片吸收或吸附。

When comparing the results of our experiment with those of Ma et al. (2001), who showed P. vittata could hyperaccumulate As from a soil containing less As than the highest treatment in this trial, it is clear that our ferns have no specialised As-uptake mechanism.

Ma et al.（2001）表明，P. vittata能够从As含量低于本试验最高处理的土壤中超富集As。将本试验结果与之比较可知，本研究中的蕨类植物显然不具备特化的As吸收机制。

4.2. Mechanisms of As-uptake by aquatic plants4.2. 水生植物吸收As的机制

For the aquatic plants used in our experiments, As was accumulated to a greater extent in situ than under controlled conditions. This is similar to the findings of Liddle (1982) for C. demersum. These differences may be due to the chemical composition of the water, plus interactions with sediments. In the Waikato River, contamination of plant material with sediment would, on a dry weight basis, reduce the measured As concentration, as the mean As concentration is an order of magnitude lower in the sediment than in C. demersum (Table 1).

对于本试验所用的水生植物，原位条件下的As积累程度高于受控条件。这与Liddle（1982）对C. demersum的研究结果相似。这些差异可能源于水体化学组成以及与沉积物的相互作用。在怀卡托河中，由于沉积物的平均As浓度比C. demersum低一个数量级（表1），植物材料受沉积物污染会使以干重计的As实测浓度降低。

An alternative hypothesis is that suspended oxides of Fe may bind to the surface of aquatic plants and adsorb As and otherdissolvedelements.Inthiscase,Asaccumulationwould thus occur via physicochemical adsorption rather than biological uptake. The Fe concentrations in the aquatic plants in this study were well in excess of those required for metabolic processes. Salisbury and Ross (1992) report average Fe concentrations in maize and cherry leaves at 120 and 58 mg kg⁻¹, respectively. Our geometric mean was 3798 mg kg⁻¹ and the maximum value was 34,900 mg kg⁻¹ (Table 4), namely 3.5%.

另一种假说是，悬浮的铁氧化物可能结合在水生植物表面，并吸附As及其他溶解元素。在此情况下，As积累是通过物理化学吸附而非生物吸收实现的。本研究中水生植物的Fe浓度远超代谢过程所需。Salisbury and Ross（1992）报道玉米和樱桃叶片的平均Fe浓度分别为120和58 mg kg⁻¹。而本研究的几何均值为3798 mg kg⁻¹，最大值为34,900 mg kg⁻¹（表4），即3.5%。

The significant and positive correlation between As and Fe concentrations is also consistent with As being incorporated into Fe oxides attached to the surface of the plant. This phenomenon was observed by Blute et al. (2004) on the roots of Typha latifolia (cattail) growing in contaminated wetland sediments. Chen et al. (2005) demonstrated that iron plaques on the surface of rice roots not only bound As, but also promoted its uptake by the root.

As与Fe浓度之间的显著正相关也符合As被结合进附着于植物表面的铁氧化物这一推断。Blute et al.（2004）在污染湿地沉积物中生长的Typha latifolia（宽叶香蒲）根系上观察到了这一现象。Chen et al.（2005）证明，水稻根表的铁膜不仅能结合As，还能促进根系对As的吸收。

Further supporting evidence that As is surface-bound comes from the observation that As was rapidly desorbed in the depuration experiment. If As were internalised into cellular structures, then it would be expected that natural depuration would be limited. Finally, the hypothesis is supported by the observation that the total dry weight As concentrations were highest in plants with the highest surface areas (and therefore highest surface area-to-weight ratios), notably M. propinquum.

排出试验中As被迅速解吸的现象进一步证明As结合于植物表面。若As已进入细胞结构内部，则自然排出应较为有限。最后，以干重计总As浓度最高的是表面积最大（因而表面积与重量之比最高）的植物，尤其是M. propinquum，这一观察结果也支持上述假说。

When watercress was grown in soil or hydroponically, the lack of As accumulation in the aerial portions at solution concentrations similar to those found in the Waikato River and TVZ indicated that this species has no efficient Astranslocation mechanisms. At higher solution concentrations, some As accumulation in the stems and leaves occurred; however, the growth was negatively affected and the plant showed signs of necrosis. Again, this evidence is consistent with the hypothesis that there is no specific uptake or tolerance mechanism for As accumulation in watercress.

豆瓣菜在土壤或水培条件下生长时，在与怀卡托河和TVZ相近的溶液浓度下，其地上部分未积累As，表明该物种不具备高效的As转运机制。在较高溶液浓度下，茎和叶中出现一定程度的As积累，但生长受到不利影响，植株出现坏死症状。这些证据同样支持豆瓣菜不具备特定As吸收或耐受机制的假说。

4.3. Arsenic in the food chain and potential human exposure4.3. 食物链中的砷及人体潜在暴露

Plant As accumulation may facilitate the entry of this toxic element into the food chain and provide an exposure pathway to humans. The effect on humans of consuming As-rich watercress is unclear. Some local people report no ill effects, despite having consumed watercress from As-rich areas for many years. Any As toxicity from consuming watercress will depend on the amount and frequency eaten, how the watercress is prepared, what it is consumed with and the chemical form of As in the plant. In this respect, the finding that most As is likely to be adsorbed to the plant surfaces would imply that most of the As in watercress is likely to be the more toxic inorganic form. Transformation to plant organoarsenicals generally presupposes biochemical mediation.

植物对As的积累可能促进这一有毒元素进入食物链，并构成人体暴露途径。人类食用富As豆瓣菜的影响尚不明确。一些当地居民反映，尽管多年食用富As地区的豆瓣菜，但并未出现不良反应。食用豆瓣菜可能引起的As毒性取决于食用量和频率、烹饪方式、同食的其他食物以及植物中As的化学形态。就此而言，大部分As可能吸附于植物表面这一发现意味着，豆瓣菜中的As大部分可能是毒性更强的无机形态。植物体内有机砷化合物的转化通常以生化介导为前提。

For the purposes of this work, the most conservative international figure of 0.3 �g kg⁻¹ of body weight per day will be applied (DEFRA, 2002). Further, due to the likelihood that As in watercress is mostly present in a surface-adsorbed form, an assumption will be made that all of the As in the watercress is inorganic. Use of a conservative approach is standard for the initial risk-assessment of ingested dietary contaminants. The TDI may be taken as a threshold level below which adverse effects are unlikely.

本研究采用国际上最保守的数值，即每天0.3 μg kg⁻¹体重（DEFRA, 2002）。此外，鉴于豆瓣菜中的As可能主要以表面吸附形态存在，假定豆瓣菜中的As全部为无机As。采用保守方法是膳食摄入污染物初步风险评估的标准做法。TDI可视为一个阈值，低于该值时不太可能产生不良影响。

Therefore, a 70-kg person should consume no more than 0.15 mg of As per week. Assuming the person consumes watercress from Lake Ohakure, which contains an average of 9 mg kg⁻¹ As, and that this is the only source of As in the person’s diet, then they would need to consume just 16 g of fresh watercress per week to exceed the TDI. It is probable, therefore, that routine ingestion of watercress would cause a person’s total inorganic As dose to move beyond the threshold where adverse effects are unlikely, and into an area where they become more probable.

因此，一个体重70 kg的人每周As摄入量不应超过0.15 mg。假设此人食用采自Lake Ohakure的豆瓣菜（平均含As 9 mg kg⁻¹），且该豆瓣菜是其膳食中唯一的As来源，则每周仅需食用16 g新鲜豆瓣菜即会超过TDI。因此，经常食用豆瓣菜很可能使人体无机As总摄入量超出不太可能产生不良影响的阈值，进入不良影响较可能发生的范围。

The potential As-contribution from watercress is also high in relation to background levels of As in the New Zealand diet. On the basis of New Zealand total diet survey data for 1997/1998 (Vannoort et al., 2000), making a standard assumption that 10% of As in food is inorganic, the weekly ingestion of 7 g of watercress containing 9 mg kg⁻¹ As would be sufficient to double dietary intakes of inorganic As.

与新西兰膳食中As的背景水平相比，豆瓣菜对As摄入的潜在贡献也很高。根据新西兰1997/1998年总膳食调查数据（Vannoort et al., 2000），按食物中10%的As为无机As这一标准假设，每周摄入7 g含As 9 mg kg⁻¹的豆瓣菜即足以使膳食无机As摄入量翻倍。

Values of up to 138 mg kg⁻¹ As on a fresh weight basis have been found in this study, indicating that, in some cases, the TDI for As may be exceeded many-fold if the plant is consumed. However, it would require an epidemiological study to indicate any cancer risk associated with the consumption of As-rich aquatic plants. This is because it would be difficult to separate cancer caused by As from other cancer-causing activities such as smoking and excessive drinking.

本研究发现，以鲜重计As含量高达138 mg kg⁻¹，表明在某些情况下食用该植物可能使As摄入量超过TDI数倍。然而，需要开展流行病学研究才能确定食用富As水生植物是否存在致癌风险，因为很难将As导致的癌症与吸烟、过量饮酒等其他致癌行为区分开来。

The presence of other toxic heavy metals such as Sb, Hg and Tl may exacerbate As toxicity.

Sb、Hg和Tl等其他有毒重金属的存在可能加剧As的毒性。

Humans may also be exposed to As indirectly. Much of the Waikato River is surrounded by farmland, and stock occasionally have access to aquatic weeds. Fishing is popular in the region. However, a previous study (Robinson et al., 1995b) showed that As levels in fish were unlikely to pose a risk to human health.

人类还可能间接暴露于As。怀卡托河大部分河段周边为农田，牲畜偶尔可接触到水草。该地区垂钓活动盛行，但此前的一项研究（Robinson et al., 1995b）表明，鱼体中的As水平不太可能对人体健康构成风险。

In a lake or river system, the amount of plant-bound As at any one time may be a significant portion of the total amount of As in the river. If, for example, low river flows or pesticides kill the plants, then there may be a large pulse of As released into the water.

在湖泊或河流系统中，任一时刻植物结合的As量可能占河流总As量的相当大比例。例如，若河流低流量或农药导致植物死亡，则可能有大量As集中释放到水体中。

4.4. Aquatic macrophytes for the bioindication or phytoremediation of As contaminated water

4.4. 利用大型水生植物对As污染水体进行生物指示或植物修复

The bioaccumulation coefficients for the aquatic plants in this study are higher than any previously reported for terrestrial species. They may therefore be useful for the phytoremediation of As from contaminated drinking water. The possibility of using plants to remove As has been discussed by Brooks and Robinson (1998). More generally, the use of aquatic plants to remove pollutants from contaminated water has been described by Wolverton (1975) and Wolverton and McDonald (1975a,b).

本研究中水生植物的生物富集系数高于以往报道的任何陆生物种，因此可能适用于受As污染饮用水的植物修复。Brooks and Robinson（1998）已探讨过利用植物去除As的可能性。更广泛而言，Wolverton（1975）和Wolverton and McDonald（1975a,b）描述了利用水生植物去除污染水体中污染物的方法。

Alternatively, aquatic plants may be used to bioindicate the level of water-contamination. The high-As bioaccumulation coefficients would make As detection far simpler than direct measurement of the water. Robinson et al. (1995a) measured As concentrations in C. demersum and the ambient water from 25 locations along the Waikato River. There was a highly significant (r = 0.60, p < 0.01) and positive correlation between the plant As concentration and that of the ambient water. This indicates that the As concentration of the plants could be used to predict the As concentration of the river water. Moreover, the plants (average 412 mg As kg⁻¹) contained around 10 times the As concentration of the sediments (average 46 mg As kg⁻¹) that, in turn, had over 1000 times the As concentration of the ambient water (average 0.042 mg As L⁻¹).

此外，水生植物还可用于生物指示水体污染程度。高As生物富集系数使As检测远比直接测定水体更为简便。Robinson et al.（1995a）测定了怀卡托河沿岸25个地点C. demersum及其环境水体中的As浓度，发现植物As浓度与环境水体As浓度之间存在极显著正相关（r = 0.60，p < 0.01）。这表明可利用植物的As浓度预测河水的As浓度。此外，植物中的As浓度（平均412 mg As kg⁻¹）约为沉积物（平均46 mg As kg⁻¹）的10倍，而沉积物的As浓度又是环境水体（平均0.042 mg As L⁻¹）的1000倍以上。

Other factors, such as the pH, water temperature and nutrientavailabilitywilldoubtlessaffectAsaccumulation.Further work needs to be carried out on these effects to determine how well these bioindicators would perform under various scenarios.

pH、水温和养分有效性等其他因素无疑也会影响As积累。需要针对这些影响开展进一步研究，以确定这些生物指示植物在不同情境下的表现。

5Conclusions结论

We found a clear distinction in As concentrations between aquatic and terrestrial plants. Arsenic accumulation is widespread among aquatic plants, and we found concentrations of 100–1000 mg kg⁻¹ in several previously untested species. Arsenic accumulation in other aquatic species will undoubtedly be found as further surveying is conducted.

本研究发现水生植物与陆生植物的As浓度存在明显差异。砷积累在水生植物中普遍存在，我们在若干此前未经测试的物种中发现了100–1000 mg kg⁻¹的浓度。随着调查的深入，无疑还会发现其他积累As的水生物种。

Arsenic accumulation by aquatic macrophytes may make them valuable tools for the bioindication and phytoremediation of As in fresh waters. Additionally the ecological impacts of As accumulation are likely to be profound. Clearly, no aquatic plants should be consumed from waterways with geothermal inflows, or with other sources of As contamination, either by humans or livestock.

大型水生植物对As的积累可能使其成为淡水中As生物指示和植物修复的有用工具。此外，As积累的生态影响可能十分深远。显然，无论是人类还是牲畜，均不应食用采自有地热水汇入或其他As污染来源的水道中的任何水生植物。

Our experiments provide indirect evidence that As is adsorbed onto the surface of the plant via physicochemical reactions, probably as co-precipitation with Fe. This hypothesis could be confirmed by microanalyses of the tissues to determine whether As is present inside the cells or simply bound to the outer cell walls. In this latter case, it could be argued that the plants are not true hyperaccumulators, as they may lack specialised As-uptake and storage mechanisms. Nevertheless, this does not change their potential usefulness as bioindicators, or make them any less toxic if consumed.

本研究试验提供了间接证据，表明As通过物理化学反应吸附于植物表面，可能是与Fe共沉淀所致。这一假说可通过组织微区分析加以证实，以确定As是存在于细胞内部，还是仅结合在细胞外壁上。若为后者，则可以认为这些植物并非真正的超富集植物，因为它们可能缺乏特化的As吸收和贮存机制。尽管如此，这并不改变其作为生物指示植物的潜在用途，也不会降低其被食用时的毒性。

Acknowledgements致谢

We are most grateful to Prof. Mary Beth Kirkham who provided a constructive review of the manuscript. We thank Environment Waikato for financial support for this study.

衷心感谢Mary Beth Kirkham教授对本文稿提出的建设性审阅意见。感谢Environment Waikato对本研究的资助。

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