Environmental Pollution 143 (2006) 1e3 www.elsevier.com/locate/envpol
Letter to the editor
Paula Madejo´n a, Teodoro Maran˜o´n b,*, Jose´ M. Murillo b, Brett Robinson c
a School of Biological and Earth Sciences, Liverpool John Moores University, Byrom Street, Liverpool L3 3AF, UK b Instituto de Recursos Naturales y Agrobiologı´a, CSIC, P.O. Box 1052, E-41080 Sevilla, Spain
c Institut fu¨r Terrestrische O¨ kologie, Universita¨tstrasse 16, ETH Zentrum CHN F 24.1, CH-8092 Zu¨rich, Switzerland
Received 10 October 2005; accepted 3 November 2005
The use of plants as biomonitors of soil quality has important advantages, particularly on a large scale.
Abstract摘要
Biomonitors are organisms that provide quantitative information on environmental quality. There are some constraints and limitations for the use of plants as biomonitors of soil pollution, as pointed out recently by some authors in this journal. However, we defend the use of plants as biomonitors, and argue that they have important advantages over soil analyses as indicators of soil quality, particularly when investigations are made on a large scale.
生物监测体是能够提供环境质量定量信息的生物。正如近期一些作者在本刊中指出的，利用植物作为土壤污染生物监测体存在一定的制约和局限。然而，我们坚持支持以植物作为生物监测体，并认为作为土壤质量指标，植物相比土壤分析具有重要优势，尤其是在大尺度调查中。
� 2005 Elsevier Ltd. All rights reserved.
© 2005 Elsevier Ltd. 版权所有。
Keywords: Plant biomonitoring; Plantemetal interactions; Risk-based assessment; Soil quality
关键词：植物生物监测；植物–金属相互作用；基于风险的评估；土壤质量
1Introduction引言
Biomonitors are organisms that provide quantitative information on environmental quality (Bargagli, 1998; Markert et al., 2003). In a study of the plantesoil relationships in areas along the Guadiamar river, Southern Spain, that were affected by the 1998 mine tailings collapse, we concluded that the leaves of white poplar (Populus alba) could be used as biomonitors for soil Zn and Cd (Madejo´n et al., 2004).
生物监测体是能够提供环境质量定量信息的生物（Bargagli, 1998; Markert et al., 2003）。在一项针对西班牙南部Guadiamar河沿岸受1998年尾矿库溃坝影响区域植物–土壤关系的研究中，我们得出结论：银白杨（Populus alba）的叶片可用作土壤Zn和Cd的生物监测体（Madejón et al., 2004）。
In a recently-published invited paper in this journal, Mertens et al. (2005) cited our study ‘‘to illustrate some of the logical flaws which occur in the scientific literature’’. While conceding that our conclusion was correct, Mertens et al. (2005) went on to point out practical constraints and limitations of biomonitors compared to soil analyses. Briefly, they considered that plant biomonitors of soil quality were limited by five factors: (1) metal bioavailability and uptake is dependent on plant species and variety, therefore biomonitoring will be restricted to the range of that plant, (2) no single plant species responds to a wide range of contaminants, (3) leaf metal concentrations are a function of time, plant development and other environmental factors, (4) tree height can make leaf sampling difficult, and (5) roots may actively avoid metal hotspots. We accept the relevance of these points. However, we disagree with their conclusion that foliar analyses have little value for biomonitoring soil pollution. We would like to clarify the role of biomonitors as tools to measure soil quality, as distinct from the total metal concentration in the soil, which we agree, is best measured by direct soil analyses.
在本刊近期发表的一篇特邀论文中，Mertens et al. (2005)引用了我们的研究，“以说明科学文献中出现的一些逻辑缺陷”。Mertens et al. (2005)虽然承认我们的结论是正确的，但随后指出了与土壤分析相比生物监测体在实际应用中的制约和局限。简言之，他们认为土壤质量植物生物监测体受以下五个因素限制：（1）金属的生物有效性及吸收取决于植物种类和品种，因此生物监测将局限于该植物的分布范围；（2）没有任何单一植物物种能够对多种污染物作出响应；（3）叶片金属浓度是时间、植物发育阶段及其他环境因素的函数；（4）树木高度可能给叶片采样带来困难；（5）根系可能主动避开金属热点区。我们认可上述观点的合理性。然而，我们不同意其关于叶片分析对土壤污染生物监测价值甚微的结论。我们希望阐明生物监测体作为衡量土壤质量工具的作用，这有别于土壤中的金属总浓度——我们同意，后者最好通过直接的土壤分析来测定。
* Corresponding author. Tel.: +34 954624711; fax: +34 954624002.
* 通讯作者。电话：+34 954624711；传真：+34 954624002。
E-mail address: teodoro@irnase.csic.es (T. Maran˜o´n).
2Biomonitoring soil quality土壤质量的生物监测
Soil quality can be defined as ‘‘The capacity of a soil to function within ecosystem boundaries, to sustain biological productivity, maintain environmental quality, and promote plant and animal health’’ (Doran and Parkin, 1994). Obviously, we do not propound that soil analyses should be forgone. The most effective way of determining the total metal concentration in the soil at any given point is, clearly to measure it directly, as we did it in our soil-poplar study (Madejo´n et al., 2004). Biomonitors indicate soil quality. They are not an analytical method to measure the total metal concentration. Plants as biomonitors have several important advantages over soil analyses when investigating soil quality, particularly on a large scale. By definition, biomonitors exhibit the effect of metal on living organisms, thus revealing information on soil quality that is difficult to measure using direct soil analyses. Regulatory authorities are increasingly adopting a risk-based approach when assessing soil quality (e.g., Swartjes, 1999; Tarazona et al., 2005). Risk-based assessment investigates the effect of contaminants on humans and ecosystems, rather than simply using the total contaminant concentration in the soil. Here again, biomonitors provide a direct measurement of a biological effect, rather than inferring values using soil extractions.
土壤质量可定义为“土壤在生态系统范围内发挥功能、维持生物生产力、保持环境质量并促进植物和动物健康的能力”（Doran and Parkin, 1994）。显然，我们并不主张放弃土壤分析。测定任一给定点土壤中金属总浓度最有效的方法显然是直接测定，正如我们在土壤–杨树研究中所做的那样（Madejón et al., 2004）。生物监测体指示的是土壤质量，而非测定金属总浓度的分析方法。在调查土壤质量时，尤其是在大尺度上，植物作为生物监测体相比土壤分析具有若干重要优势。根据定义，生物监测体表现的是金属对生物体的效应，从而揭示了难以通过直接土壤分析获得的土壤质量信息。监管机构在评估土壤质量时越来越多地采用基于风险的方法（例如Swartjes, 1999; Tarazona et al., 2005）。基于风险的评估考察污染物对人类和生态系统的效应，而不是简单地采用土壤中污染物的总浓度。在这方面，生物监测体同样提供了对生物效应的直接测量，而非借助土壤提取来推断数值。
0269-7491/$ - see front matter � 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2005.11.008
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3Advantages of plant biomonitoring植物生物监测的优势
Consideration of the aforementioned constraints and limitations of biomonitors is essential when selecting biomonitors and interpreting data. Nevertheless, when compared to direct soil analyses, some of these apparent constraints and limitations are advantageous for evaluating soil quality. That metal bioavailability and metal uptake is a function of plant genotype (Points 1 and 2) means that a suitable plant biomonitor should be selected that best represents the risk associated with a future land use. For example, plants with a high rooteshoot transfer are the most suitable biomonitors for land that is to be used for agriculture. This can give a worstcase scenario and elucidate which areas need remediation. Conversely, the soil quality of land that is to be left as a natural ecosystem may be best assessed by biomonitoring with plant species that are the most important primary producers, and most relevant in the food web of the ecosystem.
在选择生物监测体和解释数据时，考虑上述生物监测体的制约与局限至关重要。尽管如此，与直接土壤分析相比，其中一些表面上的制约与局限反而有利于评价土壤质量。金属的生物有效性和吸收是植物基因型的函数（第1点和第2点），这意味着应选择最能代表未来土地利用相关风险的适宜植物生物监测体。例如，对于将用于农业的土地，根–茎转运能力高的植物是最适宜的生物监测体。这可以给出最不利情景，并明确哪些区域需要修复。相反，对于将保留为自然生态系统的土地，其土壤质量最好通过该生态系统中最重要的初级生产者、且在食物网中最具相关性的植物物种进行生物监测来评估。
Polluted soils do not usually contain just one contaminant, and it is unlikely that one would find a universal biomonitor for a suite of contaminants (Point 2). Therefore, more than one plant species should be used. For example, in the case of biomonitoring soils affected by the Aznalco´llar mine failure, we have studied, in addition to poplar trees, some herbaceous plants, such as Hirschfeldia incana that accumulate thallium in their flowers and fruits (Madejo´n et al., 2005). Soil contaminants are often mutually correlated, because they are derived from the same source, e.g. a mine tailings collapse. Therefore, in some cases, biomonitoring of a single contaminant can provide information on the degree and extent of the general soil pollution. Moreover, the extent that a biomonitor accumulates a contaminant may indicate its relative impact on soil quality. Caution needs to be applied when using biomonitors in this way, as the mobility of individual contaminants in soil may differ.
污染土壤通常并非只含有一种污染物，而且不太可能找到适用于一系列污染物的通用生物监测体（第2点）。因此，应采用不止一种植物物种。例如，在对受Aznalcóllar矿难影响土壤的生物监测中，除杨树外，我们还研究了一些草本植物，如在花和果实中积累铊的Hirschfeldia incana（Madejón et al., 2005）。土壤污染物往往相互关联，因为它们来源相同，例如尾矿库溃坝。因此，在某些情况下，对单一污染物的生物监测即可提供有关土壤总体污染程度和范围的信息。此外，生物监测体对某种污染物的积累程度可能指示该污染物对土壤质量的相对影响。以这种方式使用生物监测体时需谨慎，因为各污染物在土壤中的迁移性可能不同。
Plant metal uptake is affected by a plethora of variables besides the total soil metal concentration (Point 3). This limits the usefulness of a biomonitor as an analytical method to investigate the total soil metal burden, but enhances its ability to measure soil quality. Biomonitors can provide site-specific information on soil quality, as they incorporate the local environment (Wright and Welbourn, 2002). Studies on the biology of metal uptake by potential biomonitors such as poplar (Populus sp.) and willow (Salix sp.) trees (Laureysens et al., 2004) increase their usefulness by elucidating the effects of plant age and management on metal uptake. Just as soil sampling requires a spade or auger, there is no special difficulty in sampling tree leaves from varying parts of the canopies using a pole pruner or similar device (Point 4).
除土壤金属总浓度外，植物对金属的吸收还受众多变量影响（第3点）。这限制了生物监测体作为调查土壤金属总负荷的分析方法的用途，但增强了其衡量土壤质量的能力。由于生物监测体综合反映了当地环境，它们能够提供特定场地的土壤质量信息（Wright and Welbourn, 2002）。对杨树（Populus sp.）和柳树（Salix sp.）等潜在生物监测体金属吸收生物学的研究（Laureysens et al., 2004）阐明了植株年龄和管理措施对金属吸收的影响，从而提高了其实用性。正如土壤采样需要铁锹或土钻一样，使用高枝剪或类似工具从树冠不同部位采集树叶并无特别困难（第4点）。
Roots have been demonstrated to avoid or forage (Whiting et al., 2000) contaminant hotspots (Point 5), thus knowledge of the biomonitor’s root strategy is essential to determine the presence of any hotspots on the scale of the individual plant. Ideally, such hotspots can be measured using a spatial grid of systematic soil analyses; however, this requires extensive sampling. Biomonitors are intended for large-scale screening, to distinguish heavily-contaminated from less affected areas and to detect gradients or borders for contaminated environments. For such purposes, the most widespread and well exposed plant species in the study area should be used (Bargagli, 1998).
已有研究表明，根系会避开或趋向觅取（Whiting et al., 2000）污染物热点区（第5点），因此了解生物监测体的根系策略对于确定单株植物尺度上是否存在热点区至关重要。理想情况下，可以通过空间网格的系统土壤分析来测定此类热点区，但这需要大量采样。生物监测体旨在用于大尺度筛查，以区分重度污染区与受影响较轻的区域，并识别污染环境的梯度或边界。为此，应选用研究区内分布最广、暴露最充分的植物物种（Bargagli, 1998）。
At present, the greatest limitation to the effective use of biomonitors is the lacuna in understanding the biological component of plantemetal interactions. Site investigations based on plant biomonitoring need a number of different species. Since each is specific for a limited environment and contaminant range, having a large index will provide more tools for environmental assessment. Such indices could form a database from which suitable biomonitors can be selected to address a particular environmental problem. It is therefore disingenuous to dissuade future work on the use of plants as biomonitors of soil quality, because the biomonitor knowledge-base is in its infancy. Rather, investigations should continue apace, to augment the environmental tool kit available for risk assessment.
目前，有效使用生物监测体的最大限制在于对植物–金属相互作用中生物学组分的认识不足。基于植物生物监测的场地调查需要多种不同物种。由于每种物种仅适用于有限的环境和污染物范围，建立一个庞大的索引将为环境评估提供更多工具。此类索引可构成一个数据库，从中可选择适宜的生物监测体以解决特定的环境问题。因此，正因为生物监测体知识库尚处于起步阶段，劝阻今后开展以植物作为土壤质量生物监测体的研究是有失公允的。相反，相关研究应加速推进，以扩充可用于风险评估的环境工具箱。
Acknowledgements致谢
We thank Nicholas W. Lepp for his comments on a previous version of this manuscript. The SECOVER Programme supported the use of plants as biomonitors of soil quality in the spill-affected Guadiamar valley (S Spain).
感谢Nicholas W. Lepp对本文前一版本提出的意见。SECOVER计划资助了在受泄漏影响的Guadiamar河谷（西班牙南部）利用植物作为土壤质量生物监测体的研究。
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