Eurasian Journal of Soil Science

Abstract

The aim of this work is to determine the important routes of metal uptake in earthworms to enable a better understanding of the primary source of metal uptake in the environment. Earthworms can take up chemicals from pore water and soil both by ingestion and through contact with their skin. However, it is unclear which pathway is the most important for metal uptake. An experiment was designed in which both soil chemistry and foods were artificially manipulated, producing different pools of soil lead (Pb) with different isotope compositions at a range of Pb concentrations. Earthworms (Eiseniafetida) were exposed to different lead concentrations through the addition of 500 mg/kg lead oxide (Pb3O4) to soil and 500 mg/kg lead nitrate to food (manure), with distinctly different isotopic compositions. Earthworms were also exposed to combinations of soil only and soil plus food in order to quantify the proportions of Pb taken up from each component. After acid digestion of the earthworm tissues, the Pb isotope composition of the accumulated lead in the earthworms was measured using a Thermofisher, iCAPQ, ICP-MS for 208Pb/206Pb and 207Pb/206Pb ratios measured relative to NIST SRM 981, allowing us to determine the pathway of lead uptake. Mixing calculations have been used to deconvolute the lead isotope signatures and identify the amount of lead taken up by the earthworms from the different soil pools. Differences in bioaccumulation factors and the relative amounts of lead accumulated from different pools changes as a function of concentration in the different pools. Earthworms were shown to uptake lead from bothsoil and food sources through ingestion route. Our findings suggest that a major pathway of lead uptake in earthworm species is heavily influenced by their ecology.

Keywords

Earthworms, metals, uptake, lead, isotopic

References

<p>Barley, K.P., 1959. The influence of earthworms on soil fertility II.Consumption of soil andOMby the earthworm Allolobophora caliginosa (Savigny). Australian Journal of Agricultural Research 10(2): 179 - 185</p>

<p>Becquer, T., Daı, J., Quantın, C., Lavelle, P., 2005. Sources of bioavailable trace metals for earthworms from a Zn-, Pb- and Cd-contaminated soil. Soil Biology and Biochemistry 37: 1564&ndash;1568.</p>

<p>Bolton, P.J., Phıllıpson, J., 1976. Burrowing, feeding, egestion and energy budgets of Allolobophora rosea (Savigny) (Lumbricidae). Oecologia 23: 225&ndash;245.</p>

<p>Brulle, F., Mıtta, G., Coquerelle, C., Vıeau, D., Lemıere, S., Lepretre, A., Vandenbulcke, F., 2006. Cloning and real-time PCR testing of 14 potential biomarkers in Eisenia fetida following cadmium exposure. Environmental Science and Technology 40: 2844-2850.</p>

<p>Csuros , M., Csuros, C., 2002. Environmental Sampling and Analysis for Metals, Lewis Publishers.</p>

<p>Curry, J. P., Schmıdt, O. 2007. The feeding ecology of earthworms - A review. Pedobiologia 50: 463-477.</p>

<p>Doube, B. M., Schmıdt, O., Kıllham, K., Correll, R.,1997. Influence of mineral soil on the palatability of organic matter for lumbricid earthworms: a simple food preference study. Soil Biology and Biochemistry 29: 569-575.</p>

<p>Dunger, W., 1983. Tiere im Boden, 3rd edn. A. Ziemsen Verlag. Wittenberg Lutherstadt.</p>

<p>Dymond, P., Scheu, S., Parkınson, D., 1997. Density and distribution of Dendrobaena octaedra (Lumbricidae) in aspen and pine forests in the Canadian Rocky Mountains (Alberta). Soil Biology and Biochemistry 29: 265&ndash;273.</p>

<p>Edwards, C.A., 2004. The importance of earthworms as key representatives of soil fauna. In: EDWARDS, C. A. (ed.) Earthworm Ecology. Boca Raton, Florida.</p>

<p>Hendrıksen, N.B., 1991. Gut load and food-retention time in the earthworms Lumbricus festivus and L. castaneus: a field study. Biology and Fertility of Soils 11: 170&ndash;173.</p>

<p>Hobbelen, P.H.F., Koolhaas, J.E., Van Gestel, C.A.M., 2006. Bioaccumulation of heavy metals in the earthworms Lumbricus rubellus and Aporrectodea caliginosa in relation to total and available metal concentrations in field soils. Environmental Pollution 144: 639-646.</p>

<p>Jager, D.T., 2003. Worming your way into bioavailability, modelling the uptake of organic chemicals in earthworms. PhD Thesis, University of Utrecht.</p>

<p>Jager, T., 2004 Modeling ingestion as an exposure route for organic chemicals in earthworms (Oligochaeta). Ecotoxicology and Environmental Safety 57: 30-38.</p>

<p>Jager, T., Fleuren, R.H.L.J., Roelofs, W., De Groot, A.C., 2003b. Feeding activity of the earthworm Eisenia andrei in artificial soil. Soil Biology and Biochemistry 35: 313&ndash;322.</p>

<p>Lanno, R., Wells, J., Conder, J., Bradham, K., Basta, N., 2004. The bioavailability of chemicals in soil for earthworms. Ecotoxicology and Environmental Safety 57: 39&ndash;47.</p>

<p>Lee, K., 1985. Earthworms: Their Ecology and Relationships with Soils and Land Use, Sydney, Academic Press.</p>

<p>Lee, K.E., Foster, R.C., 1991. Soil fauna and soil structure. Australian Journal of Soil Science 29: 745-775.</p>

<p>Lepp&auml;nen, M.T., Kukkonen, J.V.K., 1998. Relative importance of ingested sediment and pore water as bioaccumulation routes for pyrene to oligochaete (Lumbriculus variegatus, M&uuml;ller). Environmental Science and Technology 32: 1503-1508.</p>

<p>Lıttle, B. J., 2011. Earthworm Uptake and Sequestration of Lead in a Terrestrial Environment. PhD.</p>

<p>Lowe, C.N., Butt, K.R., 2005. Culture techniques for soil dwelling earthworms: a review. Pedobiologia 49: 401&ndash;413.</p>

<p>Lukkarı, T., 2004. Earthworm responses to metal contamination. M.Sc, Universty of Jyvaskyla.</p>

<p>Marhan, S., Scheu, S., 2005b. The influence of mineral and organic fertilisers on the growth of the endogeic earthworm Octolasion tyrtaeum (Savigny). Pedobiologia 49: 239&ndash;249.</p>

<p>Morgan, A.J.,StuRzenbaum, S.R., Wınters, C., G.W,G., Azız, N.A.A., Kılle, P., 2004. Differential metallothionein expression in earthworm (Lumbricus rubellus) tissues. Ecotoxicology and Environmental Safety 57: 11-19.</p>

<p>Peıjnenburg, W.J.G.M., Baerselman, R. De Groot, A.C., Jager, T., Posthuma, L., Van Veen, R.P.M., 1999. Relating environmental availability to bioavailability: Soil-type-dependent metal accumulation in the oligochaete Eisenia andrei. Ecotoxicology and Environmental Safety 44: 294&ndash;310.</p>

<p>Pıearce, T.G.,1978. Gut contents of some lumbricid earthworms. Pedobiologica 18: 153&ndash;157.</p>

<p>Sızmur, T., Tılston, E., Charnock, J., Roe, B., Watts, M., Hodson, M.E., 2011. Impacts of epigeic, anecic and endogeic earthworms on metal and metalloidmobility and availability. Journal of Environmental Monitoring 13: 266-273.</p>

<p>Spurgeon, D.J., Hopkın, S.P., 1999. Comparisons of metal accumulation and excretion kinetics in earthworms (Eisenia fetida) exposed to contaminated field and laboratory soils. Applied Soil Ecoogy 11: 227-243.</p>

<p>Van Gestel, C.A.M., 2008. Physico-chemical and biological parameters determine metal bioavailability in soils. Science of the Total Environment 406: 385-395.</p>

<p>Van Gestel, C.A.M., Mol, S., 2003. The influence of soil characteristics on cadmium toxicity for Folsomia candida (Collembola: Isotomidae). Pedobiologia 47: 387-395.</p>

<p>Vıarengo, A., Sforzını, S., Moore, M. N., Boerı, M., Benfenatı, E., Colombo, A., 2014b. Immunofluorescence detection and localization of B[a]P and TCDD in earthworm tissues. Chemosphere 107: 282&ndash;28</p>

<p>Vıljoen, S.A., Reınecke, A.R., 1992. The temperature requirements of the epigeic earthworm species Eudrilus eugeniae (Oligochaeta) a laboratory study. Soil Biology and Biochemistry 24: 1345&ndash;1350.</p>

Abstract
The aim of this work is to determine the important routes of metal uptake in earthworms to enable a better understanding of the primary source of metal uptake in the environment. Earthworms can take up chemicals from pore water and soil both by ingestion and through contact with their skin. However, it is unclear which pathway is the most important for metal uptake. An experiment was designed in which both soil chemistry and foods were artificially manipulated, producing different pools of soil lead (Pb) with different isotope compositions at a range of Pb concentrations. Earthworms (Eiseniafetida) were exposed to different lead concentrations through the addition of 500 mg/kg lead oxide (Pb3O4) to soil and 500 mg/kg lead nitrate to food (manure), with distinctly different isotopic compositions. Earthworms were also exposed to combinations of soil only and soil plus food in order to quantify the proportions of Pb taken up from each component. After acid digestion of the earthworm tissues, the Pb isotope composition of the accumulated lead in the earthworms was measured using a Thermofisher, iCAPQ, ICP-MS for 208Pb/206Pb and 207Pb/206Pb ratios measured relative to NIST SRM 981, allowing us to determine the pathway of lead uptake. Mixing calculations have been used to deconvolute the lead isotope signatures and identify the amount of lead taken up by the earthworms from the different soil pools. Differences in bioaccumulation factors and the relative amounts of lead accumulated from different pools changes as a function of concentration in the different pools. Earthworms were shown to uptake lead from bothsoil and food sources through ingestion route. Our findings suggest that a major pathway of lead uptake in earthworm species is heavily influenced by their ecology.

Keywords: Earthworms, metals, uptake, lead, isotopic

References

Barley, K.P., 1959. The influence of earthworms on soil fertility II.Consumption of soil andOMby the earthworm Allolobophora caliginosa (Savigny). Australian Journal of Agricultural Research 10(2): 179 - 185

Becquer, T., Daı, J., Quantın, C., Lavelle, P., 2005. Sources of bioavailable trace metals for earthworms from a Zn-, Pb- and Cd-contaminated soil. Soil Biology and Biochemistry 37: 1564–1568.

Bolton, P.J., Phıllıpson, J., 1976. Burrowing, feeding, egestion and energy budgets of Allolobophora rosea (Savigny) (Lumbricidae). Oecologia 23: 225–245.

Brulle, F., Mıtta, G., Coquerelle, C., Vıeau, D., Lemıere, S., Lepretre, A., Vandenbulcke, F., 2006. Cloning and real-time PCR testing of 14 potential biomarkers in Eisenia fetida following cadmium exposure. Environmental Science and Technology 40: 2844-2850.

Csuros , M., Csuros, C., 2002. Environmental Sampling and Analysis for Metals, Lewis Publishers.

Curry, J. P., Schmıdt, O. 2007. The feeding ecology of earthworms - A review. Pedobiologia 50: 463-477.

Doube, B. M., Schmıdt, O., Kıllham, K., Correll, R.,1997. Influence of mineral soil on the palatability of organic matter for lumbricid earthworms: a simple food preference study. Soil Biology and Biochemistry 29: 569-575.

Dunger, W., 1983. Tiere im Boden, 3rd edn. A. Ziemsen Verlag. Wittenberg Lutherstadt.

Dymond, P., Scheu, S., Parkınson, D., 1997. Density and distribution of Dendrobaena octaedra (Lumbricidae) in aspen and pine forests in the Canadian Rocky Mountains (Alberta). Soil Biology and Biochemistry 29: 265–273.

Edwards, C.A., 2004. The importance of earthworms as key representatives of soil fauna. In: EDWARDS, C. A. (ed.) Earthworm Ecology. Boca Raton, Florida.

Hendrıksen, N.B., 1991. Gut load and food-retention time in the earthworms Lumbricus festivus and L. castaneus: a field study. Biology and Fertility of Soils 11: 170–173.

Hobbelen, P.H.F., Koolhaas, J.E., Van Gestel, C.A.M., 2006. Bioaccumulation of heavy metals in the earthworms Lumbricus rubellus and Aporrectodea caliginosa in relation to total and available metal concentrations in field soils. Environmental Pollution 144: 639-646.

Jager, D.T., 2003. Worming your way into bioavailability, modelling the uptake of organic chemicals in earthworms. PhD Thesis, University of Utrecht.

Jager, T., 2004 Modeling ingestion as an exposure route for organic chemicals in earthworms (Oligochaeta). Ecotoxicology and Environmental Safety 57: 30-38.

Jager, T., Fleuren, R.H.L.J., Roelofs, W., De Groot, A.C., 2003b. Feeding activity of the earthworm Eisenia andrei in artificial soil. Soil Biology and Biochemistry 35: 313–322.

Lanno, R., Wells, J., Conder, J., Bradham, K., Basta, N., 2004. The bioavailability of chemicals in soil for earthworms. Ecotoxicology and Environmental Safety 57: 39–47.

Lee, K., 1985. Earthworms: Their Ecology and Relationships with Soils and Land Use, Sydney, Academic Press.

Lee, K.E., Foster, R.C., 1991. Soil fauna and soil structure. Australian Journal of Soil Science 29: 745-775.

Leppänen, M.T., Kukkonen, J.V.K., 1998. Relative importance of ingested sediment and pore water as bioaccumulation routes for pyrene to oligochaete (Lumbriculus variegatus, Müller). Environmental Science and Technology 32: 1503-1508.

Lıttle, B. J., 2011. Earthworm Uptake and Sequestration of Lead in a Terrestrial Environment. PhD.

Lowe, C.N., Butt, K.R., 2005. Culture techniques for soil dwelling earthworms: a review. Pedobiologia 49: 401–413.

Lukkarı, T., 2004. Earthworm responses to metal contamination. M.Sc, Universty of Jyvaskyla.

Marhan, S., Scheu, S., 2005b. The influence of mineral and organic fertilisers on the growth of the endogeic earthworm Octolasion tyrtaeum (Savigny). Pedobiologia 49: 239–249.

Morgan, A.J.,StuRzenbaum, S.R., Wınters, C., G.W,G., Azız, N.A.A., Kılle, P., 2004. Differential metallothionein expression in earthworm (Lumbricus rubellus) tissues. Ecotoxicology and Environmental Safety 57: 11-19.

Peıjnenburg, W.J.G.M., Baerselman, R. De Groot, A.C., Jager, T., Posthuma, L., Van Veen, R.P.M., 1999. Relating environmental availability to bioavailability: Soil-type-dependent metal accumulation in the oligochaete Eisenia andrei. Ecotoxicology and Environmental Safety 44: 294–310.

Pıearce, T.G.,1978. Gut contents of some lumbricid earthworms. Pedobiologica 18: 153–157.

Sızmur, T., Tılston, E., Charnock, J., Roe, B., Watts, M., Hodson, M.E., 2011. Impacts of epigeic, anecic and endogeic earthworms on metal and metalloidmobility and availability. Journal of Environmental Monitoring 13: 266-273.

Spurgeon, D.J., Hopkın, S.P., 1999. Comparisons of metal accumulation and excretion kinetics in earthworms (Eisenia fetida) exposed to contaminated field and laboratory soils. Applied Soil Ecoogy 11: 227-243.

Van Gestel, C.A.M., 2008. Physico-chemical and biological parameters determine metal bioavailability in soils. Science of the Total Environment 406: 385-395.

Van Gestel, C.A.M., Mol, S., 2003. The influence of soil characteristics on cadmium toxicity for Folsomia candida (Collembola: Isotomidae). Pedobiologia 47: 387-395.

Vıarengo, A., Sforzını, S., Moore, M. N., Boerı, M., Benfenatı, E., Colombo, A., 2014b. Immunofluorescence detection and localization of B[a]P and TCDD in earthworm tissues. Chemosphere 107: 282–28

Vıljoen, S.A., Reınecke, A.R., 1992. The temperature requirements of the epigeic earthworm species Eudrilus eugeniae (Oligochaeta) a laboratory study. Soil Biology and Biochemistry 24: 1345–1350.