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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
+ Author Affiliations
- Author Affiliations

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 https://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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlyhtL%2FP&md5=a8a5454d70978de5af6ee6d145a26961CAS | 20000512PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yktr7M&md5=b3977061ab625444afef30ec0a3da937CAS | 22038832PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVKrsbw%3D&md5=b1d730df43c335581f031cec34ef2334CAS | 18425578PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVKrsbo%3D&md5=a62bb12c9914b0dad31c7f2e5f71330bCAS | 18408994PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yksbfE&md5=f552a5dff9140387a5ff7b612264b8a1CAS | 22002667PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVersLjJ&md5=66bb5f70ddef5f791cd00b10e5afac24CAS | 19086204PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yksbfL&md5=d4cb74111fdb6a76fe2d7775f5fed067CAS | 22162122PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1GmtLfE&md5=12e72f628949c7fbc61224037e2ed2c2CAS | 22573562PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtFKqur0%3D&md5=b8a7ea945f5784a590834cff3bc6c1a9CAS | 21405081PubMed |

[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 | GoogleScholarGoogle Scholar | 22265985PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFeru7g%3D&md5=9cd183bcb136f8cff4361a4f577061ccCAS | 21783986PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFSgsLY%3D&md5=9fd97a466223217862ab28a206c67a0eCAS | 21499624PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVGrtLvF&md5=a89a2431443042f1b44e2bab54f2c24cCAS | 23727569PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2rsbbP&md5=4442a8338b17df7baeb4fcd7fc155053CAS | 20929986PubMed |

[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 | GoogleScholarGoogle Scholar | 22797055PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlCktrfO&md5=85450cee86579449329ee846d52ff16eCAS | 23977004PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlans7bK&md5=41baf7b13703a6dd78f48f1567c75916CAS | 20964359PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlCgtrg%3D&md5=14f45907fef3cd41f36d9a439f10d7b3CAS | 23352517PubMed |

[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 | GoogleScholarGoogle Scholar | 20384348PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktlKgsLw%3D&md5=8c3cc4c2688faf3268f8a3afbec7fdf4CAS |

[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 | GoogleScholarGoogle Scholar | 22088500PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGks7g%3D&md5=47d2fe4b925450492f1b5402cca580e2CAS | 20952651PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVKltrY%3D&md5=aa677a3edcdda6e146270f4dc9a9cfe9CAS | 21787599PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVWit7jM&md5=8c1499a5f6f1adcc23663062ec011b96CAS | 24372151PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVeisLc%3D&md5=7d55f2cb9a09cb64deb5322b3e7ebfc0CAS | 21428445PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnt1Sis70%3D&md5=7b77c1e45577cad3434c47fbcf05e90aCAS | 23664411PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFOlurY%3D&md5=e34fa31cb294534803b1b10143c51739CAS |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlslOjsLk%3D&md5=9d9d2c6ac289479cc709112aa6d11c29CAS | 18605590PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVKlu7zL&md5=1818e9ad7dbd879f808dae73c63d0bc0CAS | 21284291PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFels7vN&md5=e2bbe59c0b42b006fed00f1de07a1bd4CAS | 23739012PubMed |

[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 | GoogleScholarGoogle Scholar |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjslCisbo%3D&md5=533ef6de0b22dc5b29300afa32389c4fCAS | 10097045PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsV2qsLc%3D&md5=ba8dd6e2b796bf77acad3c604522f649CAS |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntVOitbs%3D&md5=cf285599c778bdef8aadfc0e0a6216dbCAS |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVOms70%3D&md5=68dd357c2ebf62c134bf8655d571d26dCAS | 15559278PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvFCrs7w%3D&md5=997a74badc0fb6debf800c1cf5848903CAS | 23473697PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslyqtrrM&md5=3c1152b33f7b8f59c0d587b60c9dac1dCAS | 24245665PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVWnurc%3D&md5=fe93e8c59fafcfb8247c6a2c8ae6f286CAS | 21440301PubMed |

[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 | GoogleScholarGoogle Scholar | 16002369PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFGjsbw%3D&md5=1613458857fb3801f0bac3abba5027deCAS | 20821608PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktFSrt7c%3D&md5=57b00788b8bca3f4f643e2b78d215627CAS | 15092890PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVSjtLjK&md5=899f8297d2bf6114ff2258f486e55f8aCAS | 18845859PubMed |

[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 |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvVehtrc%3D&md5=f3c09e533085cb1d3669345cc142fc7aCAS | 11482653PubMed |

[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 | GoogleScholarGoogle Scholar |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksVags7w%3D&md5=d370bd320db5204d5d65c4b617dea7d9CAS | 12143937PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht12lsA%3D%3D&md5=fec7191171ecb259ad7b0b2321864a70CAS | 20050652PubMed |

[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 | GoogleScholarGoogle Scholar |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFehtLzJ&md5=f85648260696839cb3de98de7dbae0a0CAS | 21724309PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnt12qt78%3D&md5=ee462b2ccfab70ab636298cff8dadfbcCAS | 22394349PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXltF2qt7w%3D&md5=795796ffb04924c1abde763e66aec849CAS | 24318461PubMed |

[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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1KgsL%2FO&md5=6e448bc5a5c0e86e520799f39802745dCAS | 22893546PubMed |