Environmental Chemistry Environmental Chemistry Society
Environmental problems - Chemical approaches
RESEARCH FRONT

Toxicity of cerium oxide nanoparticles to the earthworm Eisenia fetida: subtle effects

Elma Lahive A D , Kerstin Jurkschat B , Benjamin J. Shaw C , Richard D. Handy C , David J. Spurgeon A and Claus Svendsen A

A NERC Centre for Ecology and Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire, OX10 8BB, UK.

B Department of Materials, Oxford University, Begbroke Science Park, Sandy Lane, Yarnton, Oxford, OX5 1PF, UK.

C Ecotoxicology Research and Innovation Centre, Plymouth University, Drake Circus, Plymouth PL4 8AA, UK.

D Corresponding author. Email: elmhiv@ceh.ac.uk

Environmental Chemistry 11(3) 268-278 http://dx.doi.org/10.1071/EN14028
Submitted: 4 February 2014  Accepted: 16 April 2014   Published: 24 June 2014

Environmental context. This study investigates the toxicity of cerium oxide nanoparticles to earthworms, key organisms in soil ecosystems. Cerium oxide did not affect survival or reproduction of the earthworms but did exert histological changes. We conclude that current soil guidelines, based simply on metal toxicity, appear to adequately protect against cerium exposure risk, at least for earthworms.

Abstract. The toxicity of cerium oxide (CeO2) nanoparticles (NPs) in soils is largely unknown. This study aimed to investigate the toxicity of three different CeO2 NPs to the earthworm, Eisenia fetida, for effects on survival (at day 28) and reproduction (at day 56), as well as bioaccumulation and histopathological effects. Eisenia fetida were exposed in standard Lufa 2.2 soil to three CeO2 NPs of different size ranges (5–80 nm), one larger particle (300 nm) and a cerium salt (ammonium cerium nitrate) over an exposure range from 41–10 000 mg Ce kg–1. Survival and reproduction were not affected by the four CeO2 particles, even at the highest exposure concentration tested. Alternatively, 10 000 mg Ce kg–1 cerium salt affected survival and reproduction; Median lethal concentration (LC50) and effective concentration (EC50) values were 317.8 and 294.6 mg Ce kg–1. Despite a lack of toxic effect from the different forms of CeO2 particles, there was a dose-dependent increase in cerium in the organisms at all exposure concentrations, and for all material types. Earthworms exposed to CeO2 particles had higher concentrations of total cerium compared to those exposed to ionic cerium, but without exhibiting the same toxic effect. Histological observations in earthworms exposed to the particulate forms of CeO2 did, however, show cuticle loss from the body wall and some loss of gut epithelium integrity. The data suggest that that CeO2 NPs do not affect survival or reproduction in E. fetida over the standard test period. However, there were histological changes that could indicate possible deleterious effects over longer-term exposures.

Additional keyword: histopathology.


References

[1]  F. Gottschalk, T. Sonderer, R. W. Scholz, B. Nowack, Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ. Sci. Technol. 2009, 43, 9216.
Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions.CrossRef | 1:CAS:528:DC%2BD1MXhtlyhtL%2FP&md5=a8a5454d70978de5af6ee6d145a26961CAS | 20000512PubMed | open url image1

[2]  B. Nowack, J. F. Ranville, S. Diamond, J. A. Gallego-Urrea, C. Metcalfe, J. Rose, N. Horne, A. A. Koelmans, S. J. Klaine, Potential scenarios for nanomaterial release and subsequent alteration in the environment. Environ. Toxicol. Chem. 2012, 31, 50.
Potential scenarios for nanomaterial release and subsequent alteration in the environment.CrossRef | 1:CAS:528:DC%2BC3MXhs1yktr7M&md5=b3977061ab625444afef30ec0a3da937CAS | 22038832PubMed | open url image1

[3]  A. Baun, N. Hartmann, K. Grieger, K. O. Kusk, Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing. Ecotoxicology 2008, 17, 387.
Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing.CrossRef | 1:CAS:528:DC%2BD1cXmsVKrsbw%3D&md5=b1d730df43c335581f031cec34ef2334CAS | 18425578PubMed | open url image1

[4]  R. D. Handy, R. Owen, E. Valsami-Jones, The ecotoxicology of nanoparticles and nanomaterials: current status, knowledge gaps, challenges, and future needs. Ecotoxicology 2008, 17, 315.
The ecotoxicology of nanoparticles and nanomaterials: current status, knowledge gaps, challenges, and future needs.CrossRef | 1:CAS:528:DC%2BD1cXmsVKrsbo%3D&md5=a62bb12c9914b0dad31c7f2e5f71330bCAS | 18408994PubMed | open url image1

[5]  R. D. Handy, G. Cornelis, T. F. Fernandes, O. Tsyusko, A. Decho, T. Sabo-Attwood, C. Metcalfe, J. Steevens, S. J. Klaine, A. A. Koelmans, N. Horne, Ecotoxicity test methods for engineered nanomaterials: practical experiences and recommendations from the bench. Environ. Toxicol. Chem. 2012, 31, 15.
Ecotoxicity test methods for engineered nanomaterials: practical experiences and recommendations from the bench.CrossRef | 1:CAS:528:DC%2BC3MXhs1yksbfE&md5=f552a5dff9140387a5ff7b612264b8a1CAS | 22002667PubMed | open url image1

[6]  S. J. Klaine, P. J. J. Alvarez, G. E. Batley, T. F. Fernandes, R. D. Handy, D. Y. Lyon, S. Mahendra, M. J. McLaughlin, J. R. Lead, Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ. Toxicol. Chem. 2008, 27, 1825.
Nanomaterials in the environment: behavior, fate, bioavailability, and effects.CrossRef | 1:CAS:528:DC%2BD1cXhtVersLjJ&md5=66bb5f70ddef5f791cd00b10e5afac24CAS | 19086204PubMed | open url image1

[7]  S. J. Klaine, A. A. Koelmans, N. Horne, S. Carley, R. D. Handy, L. Kapustka, B. Nowack, F. von der Kammer, Paradigms to assess the environmental impact of manufactured nanomaterials. Environ. Toxicol. Chem. 2012, 31, 3.
Paradigms to assess the environmental impact of manufactured nanomaterials.CrossRef | 1:CAS:528:DC%2BC3MXhs1yksbfL&md5=d4cb74111fdb6a76fe2d7775f5fed067CAS | 22162122PubMed | open url image1

[8]  P. S. Tourinho, C. A. van Gestel, S. Lofts, C. Svendsen, A. M. Soares, S. Loureiro, Metal-based nanoparticles in soil: fate, behavior, and effects on soil invertebrates. Environ. Toxicol. Chem. 2012, 31, 1679.
Metal-based nanoparticles in soil: fate, behavior, and effects on soil invertebrates.CrossRef | 1:CAS:528:DC%2BC38Xhs1GmtLfE&md5=12e72f628949c7fbc61224037e2ed2c2CAS | 22573562PubMed | open url image1

[9]  G. Cornelis, B. Ryan, M. J. McLaughlin, J. K. Kirby, D. Beak, D. Chittleborough, Solubility and batch retention of CeO2 nanoparticles in soils. Environ. Sci. Technol. 2011, 45, 2777.
Solubility and batch retention of CeO2 nanoparticles in soils.CrossRef | 1:CAS:528:DC%2BC3MXjtFKqur0%3D&md5=b8a7ea945f5784a590834cff3bc6c1a9CAS | 21405081PubMed | open url image1

[10]  F. Gómez-Rivera, J. A. Field, D. Brown, R. Sierra-Alvarez, Fate of cerium dioxide (CeO2) nanoparticles in municipal wastewater during activated sludge treatment. Bioresour. Technol. 2012, 108, 300.
Fate of cerium dioxide (CeO2) nanoparticles in municipal wastewater during activated sludge treatment.CrossRef | 22265985PubMed | open url image1

[11]  S.-W. Lee, S.-M. Kim, J. Choi, Genotoxicity and ecotoxicity assays using the freshwater crustacean Daphnia magna and the larva of the aquatic midge Chironomus riparius to screen the ecological risks of nanoparticle exposure. Environ. Toxicol. Pharmacol. 2009, 28, 86.
Genotoxicity and ecotoxicity assays using the freshwater crustacean Daphnia magna and the larva of the aquatic midge Chironomus riparius to screen the ecological risks of nanoparticle exposure.CrossRef | 1:CAS:528:DC%2BD1MXmtFeru7g%3D&md5=9cd183bcb136f8cff4361a4f577061ccCAS | 21783986PubMed | open url image1

[12]  B. K. Gaiser, A. Biswas, P. Rosenkranz, M. A. Jepson, J. R. Lead, V. Stone, C. R. Tyler, T. F. Fernandes, Effects of silver and cerium dioxide micro- and nano-sized particles on Daphnia magna. J. Environ. Monit. 2011, 13, 1227.
Effects of silver and cerium dioxide micro- and nano-sized particles on Daphnia magna.CrossRef | 1:CAS:528:DC%2BC3MXlsFSgsLY%3D&md5=9fd97a466223217862ab28a206c67a0eCAS | 21499624PubMed | open url image1

[13]  N. Manier, A. Bado-Nilles, P. Delalain, O. Aguerre-Chariol, P. Pandard, Ecotoxicity of non-aged and aged CeO2 nanomaterials towards freshwater microalgae. Environ. Pollut. 2013, 180, 63.
Ecotoxicity of non-aged and aged CeO2 nanomaterials towards freshwater microalgae.CrossRef | 1:CAS:528:DC%2BC3sXhtVGrtLvF&md5=a89a2431443042f1b44e2bab54f2c24cCAS | 23727569PubMed | open url image1

[14]  I. Rodea-Palomares, K. Boltes, F. Fernández-Piñas, F. Leganés, E. García-Calvo, J. Santiago, R. Rosal, Physicochemical characterization and ecotoxicological assessment of CeO2 nanoparticles using two aquatic microorganisms. Toxicol. Sci. 2011, 119, 135.
Physicochemical characterization and ecotoxicological assessment of CeO2 nanoparticles using two aquatic microorganisms.CrossRef | 1:CAS:528:DC%2BC3cXhsF2rsbbP&md5=4442a8338b17df7baeb4fcd7fc155053CAS | 20929986PubMed | open url image1

[15]  I. Rodea-Palomares, S. Gonzalo, J. Santiago-Morales, F. Leganés, E. García-Calvo, R. Rosal, F. Fernández-Piñas, An insight into the mechanisms of nanoceria toxicity in aquatic photosynthetic organisms. Aquat. Toxicol. 2012, 122–123, 133.
An insight into the mechanisms of nanoceria toxicity in aquatic photosynthetic organisms.CrossRef | 22797055PubMed | open url image1

[16]  E. Artells, J. Issartel, M. Auffan, D. Borschneck, A. Thill, M. Tella, L. Brousset, J. Rose, J. Bottero, A. Thiéry, Exposure to cerium dioxide nanoparticles differently affect swimming performance and survival in two daphnid species. PLoS ONE 2013, 8, e71260.
Exposure to cerium dioxide nanoparticles differently affect swimming performance and survival in two daphnid species.CrossRef | 1:CAS:528:DC%2BC3sXhtlCktrfO&md5=85450cee86579449329ee846d52ff16eCAS | 23977004PubMed | open url image1

[17]  K. Birbaum, R. Brogioli, M. Schellenberg, E. Martinoia, W. J. Stark, D. Gonther, L. K. Limbach, No evidence for cerium dioxide nanoparticle translocation in maize plants. Environ. Sci. Technol. 2010, 44, 8718.
No evidence for cerium dioxide nanoparticle translocation in maize plants.CrossRef | 1:CAS:528:DC%2BC3cXhtlans7bK&md5=41baf7b13703a6dd78f48f1567c75916CAS | 20964359PubMed | open url image1

[18]  F. Schwabe, R. Schulin, L. K. Limbach, W. Stark, D. Bürge, B. Nowack, Influence of two types of organic matter on interaction of CeO2 nanoparticles with plants in hydroponic culture. Chemosphere 2013, 91, 512.
Influence of two types of organic matter on interaction of CeO2 nanoparticles with plants in hydroponic culture.CrossRef | 1:CAS:528:DC%2BC3sXhtlCgtrg%3D&md5=14f45907fef3cd41f36d9a439f10d7b3CAS | 23352517PubMed | open url image1

[19]  M. L. López-Moreno, G. de la Rosa, J. A. Hernández-Viezcas, H. Castillo-Michel, C. E. Botez, J. R. Peralta-Videa, J. L. Gardea-Torresdey, Evidence of the differential biotransformation and genotoxicity of ZnO and CeO2 nanoparticles on soybean (Glycine max) plants. Environ. Sci. Technol. 2010, 44, 7315.
Evidence of the differential biotransformation and genotoxicity of ZnO and CeO2 nanoparticles on soybean (Glycine max) plants.CrossRef | 20384348PubMed | open url image1

[20]  L. Vittori Antisari, S. Carbone, A. Gatti, G. Vianello, P. Nannipieri, Toxicity of metal oxide (CeO2, Fe3O4, SnO2) engineered nanoparticles on soil microbial biomass and their distribution in soil. Soil Biol. Biochem. 2013, 60, 87.
Toxicity of metal oxide (CeO2, Fe3O4, SnO2) engineered nanoparticles on soil microbial biomass and their distribution in soil.CrossRef | 1:CAS:528:DC%2BC3sXktlKgsLw%3D&md5=8c3cc4c2688faf3268f8a3afbec7fdf4CAS | open url image1

[21]  A. García, L. Delgado, J. A. Torà, E. Casals, E. González, V. Puntes, X. Font, J. Carrera, A. Sánchez, Effect of cerium dioxide, titanium dioxide, silver, and gold nanoparticles on the activity of microbial communities intended in wastewater treatment. J. Hazard. Mater. 2012, 199–200, 64.
Effect of cerium dioxide, titanium dioxide, silver, and gold nanoparticles on the activity of microbial communities intended in wastewater treatment.CrossRef | 22088500PubMed | open url image1

[22]  D. A. Pelletier, A. K. Suresh, G. A. Holton, C. K. McKeown, W. Wang, B. Gu, N. P. Mortensen, D. P. Allison, D. C. Joy, M. R. Allison, S. D. Brown, T. J. Phelps, M. J. Doktycz, Effects of engineered cerium oxide nanoparticles on bacterial growth and viability. Appl. Environ. Microbiol. 2010, 76, 7981.
Effects of engineered cerium oxide nanoparticles on bacterial growth and viability.CrossRef | 1:CAS:528:DC%2BC3MXhtFGks7g%3D&md5=47d2fe4b925450492f1b5402cca580e2CAS | 20952651PubMed | open url image1

[23]  J.-Y. Roh, Y.-K. Park, K. Park, J. Choi, Ecotoxicological investigation of CeO2 and TiO2 nanoparticles on the soil nematode Caenorhabditis elegans using gene expression, growth, fertility, and survival as endpoints. Environ. Toxicol. Pharmacol. 2010, 29, 167.
Ecotoxicological investigation of CeO2 and TiO2 nanoparticles on the soil nematode Caenorhabditis elegans using gene expression, growth, fertility, and survival as endpoints.CrossRef | 1:CAS:528:DC%2BC3cXitVKltrY%3D&md5=aa677a3edcdda6e146270f4dc9a9cfe9CAS | 21787599PubMed | open url image1

[24]  B. Collin, E. Oostveen, O. Tsyusko, J. M. Unrine, Influence of natural organic matter and surface charge on the toxicity and bioaccumulation of functionalized ceria nanoparticles in Caenorhabditis elegans. Environ. Sci. Technol. 2014, 48, 1280.
Influence of natural organic matter and surface charge on the toxicity and bioaccumulation of functionalized ceria nanoparticles in Caenorhabditis elegans.CrossRef | 1:CAS:528:DC%2BC3sXitVWit7jM&md5=8c1499a5f6f1adcc23663062ec011b96CAS | 24372151PubMed | open url image1

[25]  H. Zhang, X. He, Z. Zhang, P. Zhang, Y. Li, Y. Ma, Y. Kuang, Y. Zhao, Z. Chai, Nano-CeO2 exhibits adverse effects at environmental relevant concentrations. Environ. Sci. Technol. 2011, 45, 3725.
Nano-CeO2 exhibits adverse effects at environmental relevant concentrations.CrossRef | 1:CAS:528:DC%2BC3MXjvVeisLc%3D&md5=7d55f2cb9a09cb64deb5322b3e7ebfc0CAS | 21428445PubMed | open url image1

[26]  M. Auffan, D. Bertin, P. Chaurand, C. Pailles, C. Dominici, J. Rose, J. Y. Bottero, A. Thiery, Role of molting on the biodistribution of CeO2 nanoparticles within Daphnia pulex. Water Res. 2013, 47, 3921.
Role of molting on the biodistribution of CeO2 nanoparticles within Daphnia pulex.CrossRef | 1:CAS:528:DC%2BC3sXnt1Sis70%3D&md5=7b77c1e45577cad3434c47fbcf05e90aCAS | 23664411PubMed | open url image1

[27]  W. A. Shoults-Wilson, B. C. Reinsch, O. V. Tsyusko, P. M. Bertsch, G. V. Lowry, J. M. Unrine, Role of particle size and soil type in toxicity of silver nanoparticles to earthworms. Soil Sci. Soc. Am. J. 2011, 75, 365.
Role of particle size and soil type in toxicity of silver nanoparticles to earthworms.CrossRef | 1:CAS:528:DC%2BC3MXksFOlurY%3D&md5=e34fa31cb294534803b1b10143c51739CAS | open url image1

[28]  O. Choi, Z. Hu, Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria. Environ. Sci. Technol. 2008, 42, 4583.
Size dependent and reactive oxygen species related nanosilver toxicity to nitrifying bacteria.CrossRef | 1:CAS:528:DC%2BD1cXlslOjsLk%3D&md5=9d9d2c6ac289479cc709112aa6d11c29CAS | 18605590PubMed | open url image1

[29]  J. M. Unrine, O. V. Tsyusko, S. E. Hunyadi, J. D. Judy, P. M. Bertsch, Effects of particle size on chemical speciation and bioavailability of copper to earthworms exposed to copper nanoparticles. J. Environ. Qual. 2010, 39, 1942.
Effects of particle size on chemical speciation and bioavailability of copper to earthworms exposed to copper nanoparticles.CrossRef | 1:CAS:528:DC%2BC3cXhsVKlu7zL&md5=1818e9ad7dbd879f808dae73c63d0bc0CAS | 21284291PubMed | open url image1

[30]  L. R. Heggelund, M. Diez-Ortiz, S. Lofts, E. Lahive, K. Jurkschat, J. Wojnarowicz, N. Cedergreen, D. Spurgeon, C. Svendsen, Soil pH effects on the comparative toxicity of dissolved zinc, non-nano and nano ZnO to the earthworm Eisenia fetida. Nanotoxicology 2014, 8, 559.
Soil pH effects on the comparative toxicity of dissolved zinc, non-nano and nano ZnO to the earthworm Eisenia fetida.CrossRef | 1:CAS:528:DC%2BC3sXhvFels7vN&md5=e2bbe59c0b42b006fed00f1de07a1bd4CAS | 23739012PubMed | open url image1

[31]  C. A. Edwards, P. J. Bohlen, Biology and Ecology of Earthworms, 3rd edn 1996 (Chapman & Hall: London).

[32]  P. Lavelle, T. Decaëns, M. Aubert, S. Barot, M. Blouin, F. Bureau, P. Margerie, P. Mora, J. P. Rossi, Soil invertebrates and ecosystem services. Eur. J. Soil Biol. 2006, 42, S3.
Soil invertebrates and ecosystem services.CrossRef | open url image1

[33]  Test number 222: Earthworm Reproduction Test (Eisenia fetida/Eisenia andrei) OECD Guidelines for the Testing of Chemicals, Section 2 2004 (Organization for Economic Cooperation and Development: Paris).

[34]  S. J. Traina, V. Laperche, Contaminant bioavailability in soils, sediments, and aquatic environments. Proc. Natl. Acad. Sci. USA 1999, 96, 3365.
Contaminant bioavailability in soils, sediments, and aquatic environments.CrossRef | 1:CAS:528:DyaK1MXjslCisbo%3D&md5=533ef6de0b22dc5b29300afa32389c4fCAS | 10097045PubMed | open url image1

[35]  C. E. Smit, C. A. van Gestel, Effects of soil type, prepercolation, and ageing on bioaccumulation and toxicity of zinc for the springtail Folsomia candida. Environ. Toxicol. Chem. 1998, 17, 1132.
Effects of soil type, prepercolation, and ageing on bioaccumulation and toxicity of zinc for the springtail Folsomia candida.CrossRef | 1:CAS:528:DyaK1cXjsV2qsLc%3D&md5=ba8dd6e2b796bf77acad3c604522f649CAS | open url image1

[36]  T. Speir, H. Kettles, H. Percival, A. Parshotam, Is soil acidification the cause of biochemical responses when soils are amended with heavy metal salts? Soil Biol. Biochem. 1999, 31, 1953.
Is soil acidification the cause of biochemical responses when soils are amended with heavy metal salts?CrossRef | 1:CAS:528:DyaK1MXntVOitbs%3D&md5=cf285599c778bdef8aadfc0e0a6216dbCAS | open url image1

[37]  E. Smolders, J. Buekers, I. Oliver, M. J. McLaughlin, Soil properties affecting toxicity of zinc to soil microbial properties in laboratory-spiked and field-contaminated soils. Environ. Toxicol. Chem. 2004, 23, 2633.
Soil properties affecting toxicity of zinc to soil microbial properties in laboratory-spiked and field-contaminated soils.CrossRef | 1:CAS:528:DC%2BD2cXovVOms70%3D&md5=68dd357c2ebf62c134bf8655d571d26dCAS | 15559278PubMed | open url image1

[38]  B. J. Shaw, C. S. Ramsden, A. Turner, R. D. Handy, A simplified method for determining titanium from TiO2 nanoparticles in fish tissue with a concomitant multi-element analysis. Chemosphere 2013, 92, 1136.
A simplified method for determining titanium from TiO2 nanoparticles in fish tissue with a concomitant multi-element analysis.CrossRef | 1:CAS:528:DC%2BC3sXjvFCrs7w%3D&md5=997a74badc0fb6debf800c1cf5848903CAS | 23473697PubMed | open url image1

[39]  L. Zhao, Y. Sun, J. A. Hernandez-Viezcas, A. D. Servin, J. Hong, G. Niu, J. R. Peralta-Videa, M. Duarte-Gardea, J. L. Gardea-Torresdey, Influence of CeO2 and ZnO nanoparticles on cucumber physiological markers and bioaccumulation of Ce and Zn: a life cycle study. J. Agric. Food Chem. 2013, 61, 11945.
Influence of CeO2 and ZnO nanoparticles on cucumber physiological markers and bioaccumulation of Ce and Zn: a life cycle study.CrossRef | 1:CAS:528:DC%2BC3sXhslyqtrrM&md5=3c1152b33f7b8f59c0d587b60c9dac1dCAS | 24245665PubMed | open url image1

[40]  H. L. Hooper, K. Jurkschat, A. J. Morgan, J. Bailey, A. J. Lawlor, D. J. Spurgeon, C. Svendsen, Comparative chronic toxicity of nanoparticulate and ionic zinc to the earthworm Eisenia veneta in a soil matrix. Environ. Int. 2011, 37, 1111.
Comparative chronic toxicity of nanoparticulate and ionic zinc to the earthworm Eisenia veneta in a soil matrix.CrossRef | 1:CAS:528:DC%2BC3MXnsVWnurc%3D&md5=fe93e8c59fafcfb8247c6a2c8ae6f286CAS | 21440301PubMed | open url image1

[41]  G. Oberdörster, E. Oberdörster, J. Oberdörster, Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ. Health Perspect. 2005, 113, 823.
Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles.CrossRef | 16002369PubMed | open url image1

[42]  J. G. Coleman, D. R. Johnson, J. K. Stanley, A. J. Bednar, C. A. Weiss, R. E. Boyd, J. A. Steevens, Assessing the fate and effects of nano aluminum oxide in the terrestrial earthworm, Eisenia fetida. Environ. Toxicol. Chem. 2010, 29, 1575.
Assessing the fate and effects of nano aluminum oxide in the terrestrial earthworm, Eisenia fetida.CrossRef | 1:CAS:528:DC%2BC3cXpsFGjsbw%3D&md5=1613458857fb3801f0bac3abba5027deCAS | 20821608PubMed | open url image1

[43]  D. Spurgeon, S. Hopkin, The development of genetically inherited resistance to zinc in laboratory-selected generations of the earthworm Eisenia fetida. Environ. Pollut. 2000, 109, 193.
The development of genetically inherited resistance to zinc in laboratory-selected generations of the earthworm Eisenia fetida.CrossRef | 1:CAS:528:DC%2BD3cXktFSrt7c%3D&md5=57b00788b8bca3f4f643e2b78d215627CAS | 15092890PubMed | open url image1

[44]  R. Hughes, J. Nair, G. Ho, The toxicity of ammonia/ammonium to the vermifiltration wastewater treatment process. Water Sci. Technol. 2008, 58, 1215.
The toxicity of ammonia/ammonium to the vermifiltration wastewater treatment process.CrossRef | 1:CAS:528:DC%2BD1cXhsVSjtLjK&md5=899f8297d2bf6114ff2258f486e55f8aCAS | 18845859PubMed | open url image1

[45]  D. Spurgeon, S. Hopkin, Effects of variations of the organic matter content and pH of soils on the availability and toxicity of zinc to the earthworm Eisenia fetida. Pedobiologia 1996, 40, 80.
| 1:CAS:528:DyaK28XisV2kt70%3D&md5=89d708bb8bf38763d3f3c90df093c9a5CAS | open url image1

[46]  X. Cao, Y. Chen, X. Wang, X. Deng, Effects of redox potential and pH value on the release of rare earth elements from soil. Chemosphere 2001, 44, 655.
Effects of redox potential and pH value on the release of rare earth elements from soil.CrossRef | 1:CAS:528:DC%2BD3MXkvVehtrc%3D&md5=f3c09e533085cb1d3669345cc142fc7aCAS | 11482653PubMed | open url image1

[47]  P. R. Paquin, J. W. Gorsuch, S. Apte, G. E. Batley, K. C. Bowles, P. G. C. Campbell, C. G. Delos, D. M. Di Toro, R. L. Dwyer, F. Galvez, R. W. Gensemer, G. G. Goss, C. Hogstrand, C. R. Janssen, J. C. McGeer, R. B. Naddy, R. C. Playle, R. C. Santore, U. Schneider, W. A. Stubblefield, C. M. Wood, K. B. Wu, The biotic ligand model: a historical overview. Comp. Biochem. Physiol. Part Toxicol. Pharmacol. 2002, 133, 3.
The biotic ligand model: a historical overview.CrossRef | open url image1

[48]  X. Hu, Z. Ding, Y. Chen, X. Wang, L. Dai, Bioaccumulation of lanthanum and cerium and their effects on the growth of wheat (Triticum aestivum L.) seedlings. Chemosphere 2002, 48, 621.
Bioaccumulation of lanthanum and cerium and their effects on the growth of wheat (Triticum aestivum L.) seedlings.CrossRef | 1:CAS:528:DC%2BD38XksVags7w%3D&md5=d370bd320db5204d5d65c4b617dea7d9CAS | 12143937PubMed | open url image1

[49]  B. D. Johnston, T. M. Scown, J. Moger, S. A. Cumberland, M. Baalousha, K. Linge, R. van Aerle, K. Jarvis, J. R. Lead, C. R. Tyler, Bioavailability of nanoscale metal oxides TiO2, CeO2, and ZnO to fish. Environ. Sci. Technol. 2010, 44, 1144.
Bioavailability of nanoscale metal oxides TiO2, CeO2, and ZnO to fish.CrossRef | 1:CAS:528:DC%2BC3cXht12lsA%3D%3D&md5=fec7191171ecb259ad7b0b2321864a70CAS | 20050652PubMed | open url image1

[50]  C. van Gestel, E. Dirven-van Breemen, R. Baerselman, Accumulation and elimination of cadmium, chromium and zinc and effects on growth and reproduction in Eisenia andrei (Oligochaeta, Annelida). Sci. Total Environ. 1993, 134, 585.
Accumulation and elimination of cadmium, chromium and zinc and effects on growth and reproduction in Eisenia andrei (Oligochaeta, Annelida).CrossRef | open url image1

[51]  P. L. Kool, M. D. Ortiz, C. A. M. van Gestel, Chronic toxicity of ZnO nanoparticles, non-nano ZnO and ZnCl2 to Folsomia candida (Collembola) in relation to bioavailability in soil. Environ. Pollut. 2011, 159, 2713.
Chronic toxicity of ZnO nanoparticles, non-nano ZnO and ZnCl2 to Folsomia candida (Collembola) in relation to bioavailability in soil.CrossRef | 1:CAS:528:DC%2BC3MXhtFehtLzJ&md5=f85648260696839cb3de98de7dbae0a0CAS | 21724309PubMed | open url image1

[52]  M. J. Van Der Ploeg, R. D. Handy, L.-H. Heckmann, A. Van Der Hout, N. W. Van Den Brink, C60 exposure induced tissue damage and gene expression alterations in the earthworm Lumbricus rubellus. Nanotoxicology 2013, 7, 432.
C60 exposure induced tissue damage and gene expression alterations in the earthworm Lumbricus rubellus.CrossRef | 1:CAS:528:DC%2BC3sXnt12qt78%3D&md5=ee462b2ccfab70ab636298cff8dadfbcCAS | 22394349PubMed | open url image1

[53]  M. J. van der Ploeg, R. D. Handy, P. L. Waalewijn-Kool, J. H. van den Berg, Z. E. Herrera Rivera, J. Bovenschen, B. Molleman, J. M. Baveco, P. Tromp, R. J. Peters, G. F. Koopmans, I. M. Rietjens, N. W. van den Brink, Effects of silver nanoparticles (NM-300 K) on Lumbricus rubellus earthworms and particle characterisation in relevant test matrices, including soil. Environ. Toxicol. Chem. 2014, 33, 743.
Effects of silver nanoparticles (NM-300 K) on Lumbricus rubellus earthworms and particle characterisation in relevant test matrices, including soil.CrossRef | 1:CAS:528:DC%2BC2cXltF2qt7w%3D&md5=795796ffb04924c1abde763e66aec849CAS | 24318461PubMed | open url image1

[54]  A. C. Johnson, B. Park, Predicting contamination by the fuel additive cerium oxide engineered nanoparticles within the United Kingdom and the associated risks. Environ. Toxicol. Chem. 2012, 31, 2582.
Predicting contamination by the fuel additive cerium oxide engineered nanoparticles within the United Kingdom and the associated risks.CrossRef | 1:CAS:528:DC%2BC38Xhs1KgsL%2FO&md5=6e448bc5a5c0e86e520799f39802745dCAS | 22893546PubMed | open url image1



Export Citation Cited By (10)