Earthworms as biological monitors of cadmium, copper, lead and zinc in metalliferous soils

Earthworms (Lumbricus rebellus and Dendrodrilus rubidus) were sampled from one uncontaminated and fifteen metal-contaminated sites. Significant positive correlations were found between the earthworm and 'total' (conc. nitric acid-extractable) soil Cd, Cu, Pb and Zn concentrations (data log1) transformed). The relationships were linear, and the accumulation patterns for both species were similar when a single metal was considered, even though there were species difference in mean metal concentrations. Generally, the earthworm Cd concentration exceeded that of the soil; by contrast, the worm Pb concentration was lower than the soil Pb concentration in all but one (acidic, low soil Ca) site. Our observations suggest that Cu and Zn accumulation may be physiologically regulated by both species. Total-soil Cd explained 82-86% of the variability (V2) in earthworm Cd concentration; 52-58% of worm Pb and worm Zn concentrations were explained by the total-soil concentrations of the respective metals. Total-soil Cu explained only 11-32% of the worm Cu concentration. The effect of soil pH, total Ca concentration, cation-exchange capacity (CEC) and organic carbon on metal accumulation by L. rubellus and D. rubidus was investigated by multiple regression analysis. Soil pH (coupled with CEC) and soil Ca had a major influence on Pb accumulation (V2 of worm Pb increased to 77-83%), and there was some evidence that Cd accumulation may be suppressed in extremely organic soils. The edaphic factors investigated had no effect on Cu or Zn accumulation by earthworms. In the context of biomonitoring, it is proposed that earthworms have a potential in a dual role: (1) as 'quantitative' monitors of total-soil metal concentrations (as shown for Cd); and (2) as estimators of 'ecologically significant' soil metal, integrating the effects of edaphic factors (as shown for Pb).     

Heavy metal concentrations in soil and earthworms in a floodplain grassland

We determined accumulated heavy metal concentrations (Cd, Pb, Cu, Zn) of earthworms in moderately contaminated floodplain soils. Both soil and mature earthworms were sampled before and after flooding and earthworm species were identified to understand species specific differences in bioconcentration. Accumulated metal concentrations in floodplain earthworms differed before and after flooding. Differences in uptake and elimination mechanisms, in food choice and living habitat of the different earthworm species and changes in speciation of the heavy metals are possible causes for this observation. Regression equations taken from literature, that relate metal accumulation by earthworms in floodplains as a function of metal concentration in soil, performed well when all species specific data were combined in an average accumulation, but did not address differences in accumulation between earthworm species.     

Accumulation of heavy metals from polluted soils by the earthworm, Lumbricus rubellus: can laboratory exposure of 'control' worms reduce biomonitoring problems?

This paper compares the patterns of metal (Pb, Zn, Cd, Cu) accumulation in nine populations of the epigeic earthworm, Lumbricus rubellus, native on metalliferous soils, with the patterns of metal accumulation in batches of L. rubellus sampled from an uncontaminated site and maintained on the nine contaminated soils for 31 days under laboratory conditions. The primary findings were: (1) the Pb, Zn and Cd concentrations in the 'native' worms were significantly higher in most cases than in the 'introduced' worms; (2) multiple regression analyses indicated that the relationships between tissue and soil metal concentrations were similar for 'native' and 'introduced' worms; (3) high soil organic matter content reduced the bioavailability of Pb, but low pH increased Pb bioavailability. It was concluded that, although no phenotypic evidence of metal-tolerant ecotypes was obtained, the exposure of earthworms from uncontaminated soils to contaminated soils under laboratory conditions can provide meaningful integrative data concerning metal bioavailability in soils which, for biomonitoring purposes, often present formidable sampling problems.     

Earthworm communities along a gradient of urbanization

Earthworms were studied at six sites along a gradient of urbanization and their relations with several soil abiotic factors were determined. Concentrations of heavy metals, calcium and magnesium in earthworms and in soils were measured by atomic absorption spectroscopy. Strong negative correlations were detected between earthworm density and soil concentrations of cadmium and magnesium. Earthworm biomass was negatively correlated with lead, copper and zinc, and positively correlated with the distance from the centre of the city. High concentrations of Cd and Zn (concentration factors 49 and 32) were accumulated by earthworms in contrast to those of Cu and Pb (2 and 1). Relations between worm and soil concentrations of heavy metals, Ca and Mg are discussed.     

Assessing the impact of organic and inorganic amendments on the toxicity and bioavailability of a metal-contaminated soil to the earthworm Eisenia andrei

Metal-contaminated soil, from the El Arteal mining district (SE Spain), was remediated with organic (6 % compost) and inorganic amendments (8 % marble sludge) to reduce the mobility of metals and to modify its potential environmental impact. Different measures of metal bioavailability (chemical analysis; survival, growth, reproduction and bioaccumulation in the earthworm Eisenia andrei), were tested in order to evaluate the efficacy of organic and inorganic amendments as immobilizing agents in reducing metal (bio)availability in the contaminated soil. The inorganic amendment reduced water and CaCl₂-extractable concentrations of Cd, Pb, and Zn, while the organic amendment increased these concentrations compared to the untreated soil. The inorganic treatment did not significantly reduce toxicity for the earthworm E. andrei after 28 days exposure. The organic amendment however, made the metal-contaminated soil more toxic to the earthworms, with all earthworms dying in undiluted soil and completely inhibiting reproduction at concentrations higher than 25 %. This may be due to increased available metal concentrations and higher electrical conductivity in the compost-amended soil. No effects of organic and inorganic treatments on metal bioaccumulation in the earthworms were found and metal concentrations in the earthworms increased with increasing total soil concentrations.     

Risk assessment of heavy metal pollution for detritivores in floodplain soils in the Biesbosch, The Netherlands, taking bioavailability into account

Floodplains of the European rivers Rhine and Meuse are heavily polluted. We investigated the risk of heavy metal pollution (Cd, Cu, Pb, Zn) for detritivores living in a floodplain area, the Biesbosch, the Netherlands, affected by these rivers. Total soil, pore water and 0.01 M CaCl(2) extractable concentrations and concentrations in plant leaves, earthworms, isopods and millipedes were measured in two sites and compared with literature data to assess possible risks. Based on total metal concentrations in soil, serious effects on detritivores were expected. However, 0.01 M CaCl(2) extractable, pore water and plant leaf concentrations were similar to metal concentrations found in unpolluted areas. Concentrations of Cu and Cd in earthworms and Cu in millipedes were higher in the Biesbosch than in animals from reference areas. All other measured concentrations of heavy metals in earthworms, isopods and millipedes were similar to the ones found in reference areas. Despite high total soil concentrations, effects of Zn, Cu, Pb and Cd pollution on isopods are therefore not expected, while millipedes may only be affected by Cu. Since Cu and Cd levels in earthworms were increased compared to animals in unpolluted soils, this faunal group seems to be most at risk. Given the engineering role of earthworms in ecosystems, effects on the ecological functioning of floodplain soils therefore cannot be excluded.     

Heavy metal availability,bioaccessibility, and leachability in contaminated soil: effects of pig manure and earthworms

A pot experiment and a leaching experiment were conducted to investigate the effects of earthworms and pig manure on heavy metals (Cd, Pb, and Zn) immobility, in vitro bioaccessibility and leachability under simulated acid rain (SAR). Results showed manure significantly increased soil organic carbon (SOC), dissolved organic carbon (DOC), available phosphorus (AP), total N, total P and pH, and decreased CaCl₂-extractable metals and total heavy metals in water and SAR leachate. The addition of earthworms significantly increased AP (from 0.38 to 1.7 mg kg^?1), and a downward trend in CaCl₂-extractable and total leaching loss of heavy metals were observed. The combined earthworm and manure treatment decreased CaCl₂-extractable Zn, Cd, and Pb. For Na₄P₂O₇-extractable metals, Cd and Pb were decreased with increasing manure application rate. Application of earthworm alone did not contribute to the remediation of heavy metal polluted soils. Considering the effects on heavy metal immobilization and cost, the application of 6% manure was an alternative approach for treating contaminated soils. These findings provide valuable information for risk management during immobilization of heavy metals in contaminated soils.

     

Metal accumulation in the earthworm Lumbricus rubellus. Model predictions compared to field data

The mechanistic bioaccumulation model OMEGA (Optimal Modeling for Ecotoxicological Applications) is used to estimate accumulation of zinc (Zn), copper (Cu), cadmium (Cd) and lead (Pb) in the earthworm Lumbricus rubellus. Our validation to field accumulation data shows that the model accurately predicts internal cadmium concentrations. In addition, our results show that internal metal concentrations in the earthworm are less than linearly (slope<1) related to the total concentration in soil, while risk assessment procedures often assume the biota-soil accumulation factor (BSAF) to be constant. Although predicted internal concentrations of all metals are generally within a factor 5 compared to field data, incorporation of regulation in the model is necessary to improve predictability of the essential metals such as zinc and copper.     

Eisenia fetida avoidance behavior as a tool for assessing the efficiency of remediation of Pb, Zn and Cd polluted soil

Remediation by means of soil leaching with ethylenediaminetetraacetic acid (EDTA) is capable of extracting the most labile soil fractions, leaving the residual metals in biologically non-available forms. We evaluated the feasibility of the standardized earthworm (Eisenia fetida) avoidance test for assessing the efficiency of soil remediation of Pb, Zn and Cd polluted soil. Chemical extraction tests (six-step sequential extraction, toxicity characteristic leaching procedure, physiologically based extraction test, diethylenediaminepentaacetic acid extraction) indicated that the mobility, oral bioaccessibility and phytoavailability of Pb, Zn and Cd were consistently reduced. However, the avoidance test showed no significant avoidance of polluted soil in favor of that which had been remediated. Pb, Zn and Cd accumulation in E. fetida mirrored the decreasing pattern of metal potential bioavailability gained by leaching the soil with increasing EDTA concentrations. The calculated bioaccumulation factors indicated the possibility of underestimating the metal bioavailability in soil using chemical extraction tests.     

Bioaccumulation of heavy metals in terrestrial invertebrates.

In this literature study, accumulation data of metals in terrestrial invertebrates were collected and compared (Arthropoda and Lumbricidae). Based on total soil concentrations and body concentrations, regression equations were calculated for each metal (Cd, Cu, Pb and Zn) and each taxonomic group. We also tried to find out whether or not accumulation levels of metals in Lumbricidae are representative for all of the studied terrestrial invertebrates. Taxonomic groups could be ordered according to the extent of metal accumulation. Significant differences in accumulation levels of a factor 2-12 were found between taxonomic groups. Overall, metal concentrations were high in Isopoda and low in Coleoptera. The concentrations in Lumbricidae were in between. It should be kept in mind that the data for Lumbricidae were mainly derived from laboratory experiments, while the data for other groups were derived from field studies. The internal Pb, Cd and Cu concentration increased with the soil concentration for most taxonomic groups in the order Pb > Cd > Cu. Body concentrations of Zn were quite constant over a range of soil concentrations. The differences in accumulation level between taxonomic groups show the relevance of including detailed information on feeding behaviour in risk assessment for invertebrate-eating animals.     

Metal and metalloid contamination in roadside soil and wild rats around a Pb-Zn mine in Kabwe, Zambia

Metal (Cr, Co, Cu, Zn, Cd, Pb, Ni) and metalloid (As) accumulation was studied in roadside soil and wild rat (Rattus sp.) samples from near a Pb-Zn mine (Kabwe, Zambia) and the capital city of Zambia (Lusaka). The concentrations of the seven metals and As in the soil samples and Pb in the rat tissue samples were quantified using atomic absorption spectroscopy. The concentrations of Pb, Zn, Cu, Cd, and As in Kabwe soil were much higher than benchmark values. Geographic Information System analysis indicated the source of metal pollution was mining and smelting activity. Interestingly, the area south of the mine was more highly contaminated even though the prevailing wind flow was westward. Wild rats from Kabwe had much higher tissue concentrations of Pb than those from Lusaka. Their body weight and renal Pb levels were negatively correlated, which suggests that mining activity might affect terrestrial animals in Kabwe.     

Habitat type-based bioaccumulation and risk assessment of metal and As contamination in earthworms, beetles and woodlice

The present study investigated the contribution of environmental factors to the accumulation of As, Cd, Cu, Pb and Zn in earthworms, beetles and woodlice, and framed within an exposure assessment of the European hedgehog. Soil and invertebrate samples were collected in three distinct habitat types. Results showed habitat-specific differences in soil and invertebrate metal concentrations and bioaccumulation factors when normalized to soil metal concentration. Further multiple regression analysis showed residual variability (habitat differences) in bioaccumulation that could not be fully explained by differences in soil metal contamination, pH or organic carbon (OC). Therefore, the study demonstrated that in bioaccumulation studies involving terrestrial invertebrates or in risk assessment of metals, it is not sufficient to differentiate habitat types on general soil characteristics such as pH and/or OC alone. Furthermore, simple generic soil risk assessments for Cd and Cu showed that risk characterization was more accurate when performed in a habitat-specific way.     

Effects of soil properties on food web accumulation of heavy metals to the wood mouse (Apodemus sylvaticus)

Effects of soil properties on the accumulation of metals to wood mice (Apodemus sylvaticus) were evaluated at two sites with different pH and organic matter content of the soil. pH and organic matter content significantly affected accumulation of Cd, Cu, Pb and Zn in earthworms and vegetation. For Cd, Cu and Zn these effects propagated through the food web to the wood mouse. Soil-to-kidney ratios differed between sites: Cd: 0.15 versus 3.52, Cu: 0.37 versus 1.30 and Zn: 0.33-0.83. This was confirmed in model calculations for Cd and Zn. Results indicate that total soil concentrations may be unsuitable indicators for risks that metals pose to wildlife. Furthermore, environmental managers may, unintentionally, change soil properties while taking specific environmental measures. In this way they may affect risks of metals to wildlife, even without changes in total soil concentrations.     

Accumulation of heavy metals in the mole in Finland

Metal concentrations (Cu, Ni, Zn, Cd, Cr, Hg, Pb and Mo) were analysed from the liver and kidneys of moles, Talpa europaea L. (Insectivora), trapped in southern Finland on both contaminated and rural areas. In rural areas the concentrations of Cd, Cu, Zn, Pb and Mo were lower in juveniles (individuals in their first summer), except for Zn in the liver, which was lower in adults. When the animals were divided into annual classes (0-6 years), Cd and Mo concentrations in the liver increased significantly with age, while concentrations of Cu, Zn and Cr tended to decrease. Female moles had higher Pb concentrations than males, especially adult females, which also had lower levels of Cu in the liver than adult males. Moles in the metropolitan area of Helsinki clearly differed from those in rural areas in that the concentrations of heavy metals in these moles were higher (especially for the most toxic metals: Cd, Pb and Hg), and their body weight was lower. The renal concentrations of Cd in most of the moles in Helsinki exceeded the threshold that has been shown to have a nephrotoxic effect in mammals. In one subsample from Helsinki, Pb and Zn concentrations in the mole liver decreased as the distance from the highway increased. Concentrations of Pb in earthworms and several heavy metals in soil also decreased similarly in the same area. Our data indicate that Pb accumulates in moles through their diet of earthworms.     

Effects of alkaline and bioorganic amendments on cadmium,lead, zinc,and nutrient accumulation in brown rice and grain yield in acidic paddy fields contaminated with a mixture of heavy metals

Paddy soils and rice (Oryza sativa L.) contaminated by mixed heavy metals have given rise to great concern. Field experiments were conducted over two cultivation seasons to study the effects of steel slag (SS), fly ash (FA), limestone (LS), bioorganic fertilizer (BF), and the combination of SS and BF (SSBF) on rice grain yield, Cd, Pb, and Zn and nutrient accumulation in brown rice, bioavailability of Cd, Pb, and Zn in soil as well as soil properties (pH and catalase), at two acidic paddy fields contaminated with mixed heavy metals (Cd, Pb, and Zn). Compared to the controls, SS, LS, and SSBF at both low and high additions significantly elevated soil pH over both cultivation seasons. The high treatments of SS and SSBF markedly increased grain yields, the accumulation of P and Ca in brown rice and soil catalase activities in the first cultivation season. The most striking result was from SS application (4.0 t ha^?1) that consistently and significantly reduced the soil bioavailability of Cd, Pb, and Zn by 38.5–91.2 % and the concentrations of Cd and Pb in brown rice by 20.9–50.9 % in the two soils over both cultivation seasons. LS addition (4.0 t ha^?1) also markedly reduced the bioavailable Cd, Pb, and Zn in soil and the Cd concentrations in brown rice. BF remobilized soil Cd and Pb leading to more accumulation of these metals in brown rice. The results showed that steel slag was most effective in the remediation of acidic paddy soils contaminated with mixed heavy metals.     

Heavy metal accumulation by poplar in calcareous soil with various degrees of multi-metal contamination: implications for phytoextraction and phytostabilization

The object of this study was to assess the capacity of Populus alba L. var. pyramidalis Bunge for phytoremediation of heavy metals on calcareous soils contaminated with multiple metals. In a pot culture experiment, a multi-metal-contaminated calcareous soil was mixed at different ratios with an uncontaminated, but otherwise similar soil, to establish a gradient of soil metal contamination levels. In a field experiment, poplars with different stand ages (3, 5, and 7 years) were sampled randomly in a wastewater-irrigated field. The concentrations of cadmium (Cd), Cu, lead (Pb), and zinc (Zn) in the poplar tissues and soil were determined. The accumulation of Cd and Zn was greatest in the leaves of P. pyramidalis, while Cu and Pb mainly accumulated in the roots. In the pot experiment, the highest tissue concentrations of Cd (40.76 mg kg^?1), Cu (8.21 mg kg^?1), Pb (41.62 mg kg^?1), and Zn (696 mg kg^?1) were all noted in the multi-metal-contaminated soil. Although extremely high levels of Cd and Zn accumulated in the leaves, phytoextraction using P. pyramidalis may take at least 24 and 16 years for Cd and Zn, respectively. The foliar concentrations of Cu and Pb were always within the normal ranges and were never higher than 8 and 5 mg kg^?1, respectively. The field experiment also revealed that the concentrations of all four metals in the bark were significantly higher than that in the wood. In addition, the tissue metal concentrations, together with the NH₄NO₃-extractable concentrations of metals in the root zone, decreased as the stand age increased. P. pyramidalis is suitable for phytostabilization of calcareous soils contaminated with multiple metals, but collection of the litter fall would be necessary due to the relatively high foliar concentrations of Cd and Zn.     

Mercury, cadmium and lead concentrations in different ecophysiological groups of earthworms in forest soils

Bioaccumulation of Hg, Cd and Pb by eight ecophysiologically distinct earthworm species was studied in 27 polluted and uncontaminated forest soils. Lowest tissue concentrations of Hg and Cd occurred in epigeic Lumbricus rubellus and highest in endogeic Octolasion cyaneum. Soils dominated by Dendrodrilus rubidus possess a high potential of risk of Pb biomagnification for secondary predators. Bioconcentration factors (soil-earthworm) followed the sequence ranked Cd > Hg > Pb. Ordination plots of redundancy analysis were used to compare HM concentrations in earthworm tissues with soil, leaf litter and root concentrations and with soil pH and CEC. Different ecological categories of earthworms are exposed to Hg, Cd and Pb in the topsoil by atmospheric deposition and accumulate them in their bodies. Species differences in HM concentrations largely reflect differences in food selectivity and niche separation.     

Bioaccumulation in Porcellio scaber (Crustacea, Isopoda) as a measure of the EDTA remediation efficiency of metal-polluted soil

Leaching using EDTA applied to a Pb, Zn and Cd polluted soil significantly reduced soil metal concentrations and the pool of metals in labile soil fractions. Metal mobility (Toxicity Characteristic Leaching Procedure), phytoavailability (diethylenetriaminepentaacetic acid extraction) and human oral-bioavailability (Physiologically Based Extraction Test) were reduced by 85-92%, 68-91% and 88-95%, respectively. The metal accumulation capacity of the terrestrial isopod Porcellio scaber (Crustacea) was used as in vivo assay of metal bioavailability, before and after soil remediation. After feeding on metal contaminated soil for two weeks, P. scaber accumulated Pb, Zn and Cd in a concentration dependent manner. The amounts of accumulated metals were, however, higher than expected on the basis of extraction (in vitro) tests. The combined results of chemical extractions and the in vivo test with P. scaber provide a more relevant picture of the availability stripping of metals after soil remediation.     

Evaluation of surrogate measures of cadmium, lead, and zinc bioavailability to Eisenia fetida

We evaluated weak-electrolyte (0.1 M Ca(NO3)2) soil extractions and ion-exchange membranes coated with a metal chelator as measures of Cd, Pb, and Zn bioavailability in spiked artificial soil by comparing their metal availability estimates to acute lethal toxicity in the earthworm Eisenia fetida. Ca(NO3)2 extractions were precisely related to toxicity in all toxicity tests, and enabled the development of time-independent LC50S (incipient lethal-levels, ILLs) calculated using exposure levels based on extraction data. ILLs with 95% CIs for the Cd, Pb, and Zn toxicity tests were 9.8 (9.4-10.3), 1.16 (1.11-1.22), and 6.33 (6.18-6.49) Ca(NO3)2-extractable mmol metal/kg soil, respectively. Mixture toxicity of Cd, Pb, and Zn, assessed using the toxic unit (TU) approach, was 1.35 TU, suggesting additivity. Chelating ion-exchange membrane uptake was variable, and not well related to toxicity. Weak-electrolyte extractions show promise as precise, inexpensive surrogate measures of Cd, Pb, and Zn bioavailability in soil.     

Variation in the mineral composition of eggs of the snail, Helix aspersa between populations exposed to different levels of metal contamination

The eggs of terrestrial gastropods represent a major investment of resources by the parent, not least in the provision of essential metals. In this experiment 11 populations of Helix aspersa were collected from habitats with different histories of lead exposure and allowed to reproduce in the laboratory. After 4 months on a low metal diet, five four-egg samples were taken from a single clutch of each population and analysed for their metal content. Within-clutch and between population variation in the eggs were measured. No Pb or Cd was detected in any of the eggs. Both trace and essential metals show considerable variation between eggs within the same clutch. Cu levels were consistent across populations while egg Zn was closely correlated with soil Zn. Median Ca and Mg levels show little relation to soil concentrations. However, Ca provision declines with soil Pb across the populations. While the metal content of the eggs appears to be closely regulated, an interaction between Pb and Ca in the parental tissues may mediate the supply of Ca to the eggs.