Cadmium uptake by earthworms as related to the availability in the soil and the intestine (original) (raw)
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Environmental Toxicology and Chemistry, 2010
Acclimation to cadmium (Cd) levels exceeding background concentrations may influence the ability of earthworms to accumulate Cd with minimum adverse effects. In the present study, earthworms (Eisenia andrei) were acclimated by exposure to 20 mg/ kg Cd (dry wt) in Webster soil for 28 d. A 224-d bioaccumulation test was subsequently conducted with both acclimated and unacclimated worms exposed in Webster soils spiked with 20 mg/kg and 100 mg/kg Cd (dry wt). Uptake kinetics and subcellular compartmentalization of Cd were examined. Results suggest that acclimated earthworms accumulated more Cd and required a longer time to reach steady state than unacclimated worms. Most of the Cd was present in the metallothionein (MT) fraction. Cadmium in the MT fraction increased approximately linearly with time and required a relatively longer time to reach steady state than Cd in cell debris and granule fractions, which quickly reached steady state. Cadmium in the cell debris fraction is considered potentially toxic, but low steady state concentrations observed in the present study would not suggest the potential for adverse effects. Future use of earthworms in ecological risk assessment should take into consideration pre-exposure histories of the test organisms. A prolonged test period may be required for a comprehensive understanding of Cd uptake kinetics and compartmentalization.
Soil Biology & Biochemistry, 2005
To study the interaction between chemical availability in a floodplain soil and physiological compartmentalization of internalised metals, bioaccumulation experiments were performed with the earthworm Lumbricus rubellus. Uptake and elimination kinetics of Zn and Cd were determined using radioisotopes, allowing for non-destructive measurements in time and allowing flux measurements of elements under homeostatic control. Two distinct compartments could be identified in the earthworm, with different affinities for Zn and Cd. The first compartment is thought to represent the pool of loosely-bound metals, whereas the second one represents a tightly bound storage fraction. A model based on this view provided an accurate description of the data set. Turnover rates were faster for Zn than for Cd. While the looselybound metal compartment determined Zn accumulation patterns, the magnitude of Cd accumulation was dominated by the behaviour of the storage compartment. Net accumulation over 2 weeks of Fe, Ni, Cu, Zn, Cd, Pb in the earthworms was at least two times higher than the absolute amount of metals present in the pore water of the soil, except for Ca. This supports the hypothesis that replenishment of the pore water concentration by desorption of metals from solid soil particles feeds metal uptake and that bioavailability cannot be seen as a static equilibrium. It is concluded that bioaccumulation estimates should be based on fluxes and account for the physiology of internalized metals. At least two internal and external compartments are needed to describe metal kinetics in an accurate way. q
EFFECT OF pH ON METAL SPECIATION AND RESULTING METAL UPTAKE AND TOXICITY FOR EARTHWORMS
Environmental Toxicology and Chemistry, 2006
In the present study, relationships between changes in the solubility and speciation of metals in contaminated soils under different pH regimes and their toxicity to earthworms were investigated. Earthworms (Lumbricus rubellus) were exposed in a laboratory bioassay to metalliferous soils under three pH regimes: Unamended pH, pH lowered by one unit (pH Ϫ1), and pH increased by one unit (pH ϩ1). In each soil, total (hot nitric acid-extractable) and 0.01 M CaCl 2 -extractable metal concentrations were measured and soil pore-water chemistry analyzed to allow metal speciation to be modeled using the Windermere Humic Aqueous Model. Earthworm metal accumulation was determined and toxicity assessed by measuring survival and reproduction and at the molecular level by recording expression of the gene encoding metallothionein-2 (MT-2) using quantitative reverse transcriptasepolymerase chain reaction. Both metal solubility and speciation were found to be highly pH dependent. Metal accumulation in earthworms was influenced by soil concentration and, in some cases (e.g., Cd), by pH. Reproduction was affected (reduced up to 90%) by soil metal level, pH, and their interaction. Relationships between analyzed and calculated Zn concentrations and toxicity and between analyzed and calculated Cd concentrations and tissue accumulation and MT-2 expression were compared by fitting dose-response models and assessing the fit of the data. This analysis indicated that values based on a pH-adjusted free ion concentration best explained toxicity (r 2 ϭ 0.82) and accumulation (r 2 ϭ 0.54). Expression of MT-2 was, however, poorly correlated ( p Ͼ 0.05) with all analyzed and modeled soil metal concentrations.
A review of studies performed to assess metal uptake by earthworms
Earthworms perform a number of essential functions in soil; the impacts of metals on earthworms are often investigated. In this review we consider the range of earthworm species, types of soil and forms of metal for which metal uptake and accumulation have been studied, the design of these experiments and the quantitative relationships that have been derived to predict earthworm metal body burden. We conclude that there is a need for more studies on earthworm species other than Eisenia fetida in order to apply the large existing database on this earthworm to other, soil dwelling species. To aid comparisons between studies agreement is needed on standard protocols that define exposure and depuration periods and the parameters, such as soil solution composition, soil chemical and physical properties to be measured. It is recommended that more field or terrestrial model ecosystem studies using real contaminated soil rather than metal-amended artificial soils are performed.
Environmental Pollution, 2014
The aim of this study was to estimate the bioavailability of essential (Zn, Cu) and non-essential metals (Cd, Pb) to the earthworm Lumbricus rubellus exposed to soils originating from a gradient of metal pollution in Southern Poland. Metal uptake and elimination kinetics were determined and related to soils properties. Experimental results were compared with tissue metal concentrations observed in earthworms from the studied transect. Cd and Pb were intensively accumulated by the earthworms, with very slow or no elimination. Their uptake rate constants, based on 0.01 M CaCl 2 -extractable concentrations in the soils, increased with soil pH. Internal concentrations of Cu and Zn were maintained by the earthworms at a stable level, suggesting efficient regulation of these metals by the animals. The estimated uptake and elimination kinetics parameters enabled fairly accurate prediction of metal concentrations reached within a life span of L. rubellus in nature.
Method for determining toxicologically relevant cadmium residues in the earthworm Eisenia fetida
Chemosphere, 2002
We investigated a method to isolate toxicologically relevant Cd in earthworms (Eisenia fetida) exposed in a 14-d Cd bioaccumulation study. A procedure involving acid insoluble ash (AIA) content was combined with homogenization and centrifugation techniques to divide total earthworm Cd burdens into supernatant (metallothionein-bound), pellet (toxicologically active), and soil-associated Cd fractions. Whereas the supernatant fraction of the earthworm digests increased linearly throughout the exposure period (from approximately 0 to 3.59 mmol/kg), the pellet fraction reached a steady-state concentration (95% CI) of 1.2 (0.9-1.4) mmol/kg, suggesting the ability of the metallothionein detoxification system to sequester incoming Cd. The AIA method was useful for correcting earthworm Cd concentrations for ingested soil-associated Cd and observing soil ingestion, which was suppressed in Cd-spiked artificial soil (1.06 (0.57-1.55)%) compared to controls (17.25 (14.36-20.15)%). These methods may be useful in investigating soil ingestion and Cd uptake and detoxification in earthworms.
Chemosphere, 2007
The effect of two ecologically contrasting earthworm species Eisenia fetida (epigeic) and Octolasion tyrtaeum (endogeic) on the fractionation (accessed using sequential extractions), mobility (toxicity characteristic leaching procedure, TCLP) and oral bioavailability (Ruby's physiologically based extraction test, PBET) of Pb, Zn and Cd was studied before and after soil remediation with soil leaching. Twenty-step leaching, with 2.5 mmol kg À1 EDTA used in each step, removed 58.4%, 25.0% and 68.0% of initial soil Pb, Zn and Cd, respectively, shifted the fractionation of residual heavy metals toward less labile forms, and decreased their mobility by 83.7%, 80.3%, and 90.9%. Pb oral bioavailability was reduced by 3.1-times (in each stomach and intestinal phase). After soil leaching, both earthworm species enriched the carbonate soil fraction in their casts with residual Pb, and increased the Pb bioavailability in the simulated intestinal phase by a factor of 2.4 (E. fetida) and 2.8 (O. tyrtaeum). The concentration of Pb in TCLP leachate from E. fetida casts was 6.2-times higher than in the bulk of the remediated soil. These results indicate that the effect of biotic factors on the availability of heavy metals residual in soil after soil leaching requires consideration.
Environmental Pollution, 2005
Comparative analysis of life-cycle, physiological and molecular responses to Cu and Cd indicate similar responses under static and fluctuating climate regimes. Abstract Laboratory toxicity tests are usually conducted under stable ambient conditions, while exposures in ecosystems occur in a fluctuating climate. To assess how climate influences the toxicity of Cu and Cd for the earthworm Lumbricus rubellus, this study compared effects for life-cycle parameters (survival, reproduction), cellular status (lysosomal membrane stability), gene expression (transcript of the metal binding protein metallothionein-2) and tissue metal concentration measured under outdoor conditions, with the same responses under constant conditions as measured by Spurgeon et al. [Spurgeon, D.J., Svendsen, C., Weeks, J.M., Hankard, P.K., Stubberud, H.E., Kammenga, J.E., 2003. Quantifying copper and cadmium impacts on intrinsic rate of population increase in the terrestrial oligochaete Lumbricus rubellus. Environmental Toxicology and Chemistry 22, 1465e1472]. Both metals were found to significantly influence earthworm reproduction, compromise lysosomal membrane stability and induce MT-2 gene expression in the outdoor system. Comparison with physiological and life-cycle responses in the laboratory indicated similar response patterns and effect concentrations for Cu. For Cd, lysosomal membrane stability and MT-2expression showed comparable responses in both exposures. Juvenile production rate, however, gave different dose response relationships, with the EC-50 in the outdoor test approximately half that in the laboratory test. A difference in Cd accumulation was also seen. Overall, however, the comparison indicated only a marginal effect of environmental fluctuations typical for northern temperate Europe on earthworm sensitivity to the two metals. (D.J. Spurgeon), csv@ceh.ac.uk (C. Svendsen), llist@ceh.ac.uk (L.J. Lister), pkh@ceh.ac.uk (P.K. Hankard), kille@cardiff.ac.uk (P. Kille). 0269-7491/$ -see front matter Ó
Uptake kinetics of metals by the earthworm Eisenia fetida exposed to field-contaminated soils
It is well known that earthworms can accumulate metals. However, most accumulation studies focus on Cd-, Cu-, Pb- or Zn-amended soils, additionally few studies consider accumulation kinetics. Here we model the accumulation kinetics of 18 elements by Eiseniafetida, exposed to 8 metal-contaminated and 2 uncontaminated soils. Tissue metal concentration was determined after 3, 7, 14, 21, 28 and 42 days. Metal elimination rate was important in determining time to reach steady-state tissue metal concentration. Uptake flux to elimination rate ratios showed less variation and lower values for essential than for non-essential metals. In theory kinetic rate constants are dependent only on species and metal. Therefore it should be possible to predict steady-state tissue metal concentrations on the basis of very few measurements using the rate constants. However, our experiments show that it is difficult to extrapolate the accumulation kinetic constants derived using one soil to another.