Skip to main content

Advertisement

SpringerLink
Log in

Toxicity of ZnO Nanoparticles, ZnO Bulk, and ZnCl2 on Earthworms in a Spiked Natural Soil and Toxicological Effects of Leachates on Aquatic Organisms

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

The present study assessed the uptake and toxicity of ZnO nanoparticles (NPs), ZnO bulk, and ZnCl2 salt in earthworms in spiked agricultural soils. In addition, the toxicity of aqueous extracts to Daphnia magna and Chlorella vulgaris was analyzed to determine the risk of these soils to the aquatic compartment. We then investigated the distribution of Zn in soil fractions to interpret the nature of toxicity. Neither mortality nor differences in earthworm body weight were observed compared with the control. The most sensitive end point was reproduction. ZnCl2 was notably toxic in eliminating the production of cocoons. The effects induced by ZnO-NPs and bulk ZnO on fecundity were similar and lower than those of the salt. In contrast to ZnO bulk, ZnO-NPs adversely affected fertility. The internal concentrations of Zn in earthworms in the NP group were greater than those in the salt and bulk groups, although bioconcentration factors were consistently <1. No relationship was found between toxicity and internal Zn amounts in earthworms. The results from the sequential extraction of soil showed that ZnCl2 displayed the highest availability compared with both ZnO. Zn distribution was consistent with the greatest toxicity showed by the salt but not with Zn body concentrations. The soil extracts from both ZnO-NPs and bulk ZnO did not show effects on aquatic organisms (Daphnia and algae) after short-term exposure. However, ZnCl2 extracts (total and 0.45-μm filtered) were toxic to Daphnia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Baalousha M, Mancuilea A, Cumberland S, Kendall K, Lead JR (2008) Aggregations and surface properties of ions oxide NPs: influence of pH and natural organic matter. Environ Toxicol Chem 9:1875–2008

    Article  Google Scholar 

  • Bian S, Mudunkotuwa IA, Rupasinghe T, Grassain VH (2011) Aggregation and dissolution of 4 nm ZnO NPs in aqueous environments: influence of pH, ionic strength, size, and adsorption of humic acid. Langmuir 27:6059–6068

    Article  CAS  Google Scholar 

  • Bigorgne E, Foucaud L, Lapied E, Labille J, Botta CL, Sirguey C et al (2011) Ecotoxicological assessment of TiO2 byproducts on the earthworm Eisenia fetida. Environ Pollut 159:2698–2705

    Article  CAS  Google Scholar 

  • Blinova I, Ivask A, Mortimer M, Kahru A (2010) Ecotoxicity of nanoparticles of CuO and ZnO in natural water. Environ Pollut 158:41–47

    Article  CAS  Google Scholar 

  • Bystrzejewska-Piotrowska G, Asztemborska M, Giska I, Mikoszewski A (2012) Influence of earthworms on extractability of metals from soils contaminated with Al2O3, TiO2, Zn and ZnO nanoparticles and microparticles of Al2O3. Pol J Environ Stud 21:313–319

    Google Scholar 

  • Chang YN, Zhang M, Xia L, Zhang J, Xing G (2012) The toxic effects and mechanisms of CuO and ZnO nanoparticles. Materials 5:2850–2871

    Article  CAS  Google Scholar 

  • Chaudhuri PS, Pal TK, Sabysaachi N, Dey SK (2012) Effects of five earthworm species on some physic-chemical properties of soil. J Environ Biol 33:713–716

    CAS  Google Scholar 

  • Coutris C, Joner EJ, Oughton DH (2012) Aging and soil organic matter content affect the fate of silver nanoparticles in soil. Sci Total Environ 420:327–333

    Article  CAS  Google Scholar 

  • De Schamphelaere KAC, Lofts S, Janssen CR (2005) Bioavailabilty models for predicting acute and chronic toxicity of zinc to algae, daphnids, and fish in natural surface waters. Environ Toxicol Chem 24:1190–1197

    Article  Google Scholar 

  • DIN 38414-S4 (1984) Teil 4: Deutsche einheitsverfaheren zur Wasser-Abwasser und Schalammuntersuchung; Schalamm und Sediment (Gruppe S). Bestimmung der Eluierbarkeit mit Wasser (S4)

  • Fernandez D, García-Gomez C, Babin M (2013) In vitro evaluation of cellular responses induced by ZnO nanoparticles, zinc ions and bulk ZnO in fish cells. Sci Total Environ 452–453:262–274

    Article  Google Scholar 

  • Franklin NM, Rogers NJ, Apte SC, Gadd GE, Casey PS (2007) Comparative ecotoxicology of nanoparticulate ZnO, bulk ZnO and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environ Sci Technol 41:8484–8490

    Article  CAS  Google Scholar 

  • Heckmann LH, Hovgaard MB, Sutherland DS, Autrup H, Besenbacher F, Scott-Fordsmand JJ (2011) Limit-test toxicity screening of selected inorganic nanoparticles to the earthworm Eisenia fetida. Ecotoxicology 20:226–233

    Article  CAS  Google Scholar 

  • Heggelund LR, Diez-Ortiz M, Lofts S, Lahive E, Jurkschat K, Wojnarowicz J et al (2014) Soil pH effects on the comparative toxicity of dissolved zinc, non-nano and nano ZnO to the earthworm Eisenia fetida. Nanotoxicology 8(5):559–572. doi:10.3109/17435390.2013.809808

    Article  CAS  Google Scholar 

  • Heinlaan M, Ivask A, Blinova I, Dubourguier H-C, Kahru A (2008) Toxicity of nanosized and bulk ZnO, CuO and TiO2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere 71:1308–1316

    Article  CAS  Google Scholar 

  • Hooper HL, Kerstin J, Morgan AJ, Bailey J, Lawlor AJ (2011) Comparative chronic toxicity of nanoparticulate and ionic zinc to the earthworm Eisenia veneta in a soil matrix. Environ Int 37:1111–1117

    Article  CAS  Google Scholar 

  • Hu CW, Li M, Cui YB, Chen J, Yang LY (2010) Toxicological effects of TiO2 and ZnO nanoparticles in soil on earthworm Eisenia fetida. Soil Biol Biochem 42:586–591

    Article  CAS  Google Scholar 

  • Jensen J, Diao X, Scott-fordsmand JJ (2007) Sub-lethal toxicity of the antiparasitic abamectin on earthworms and the application of neutral red retention time as a biomarker. Chemosphere 68:744–750

    Article  CAS  Google Scholar 

  • Kahru A, Dubourguier HC (2010) From ecotoxicology to nanoecotoxicology. Toxicology 269:105–119

    Article  CAS  Google Scholar 

  • Kool PL, Diez-Ortiz M, van Gestel CAM (2011) Chronic toxicity of ZnO nanoparticles, non-nano ZnO and ZnCl2 to Folsomia candida (collembola) in relation to bioavailability in soil. Environ Pollut 159:2713–2719

    Article  CAS  Google Scholar 

  • Li LZ, Zhou DM, Peijnenburg WJGM, Van Gestel CAM, Jin SY, Wang YJ (2011) Toxicity of zinc oxide nanoparticles in the earthworm, Eisenia fetida and subcellular fractionation of Zn. Environ Int 37:1098–1104

    Article  CAS  Google Scholar 

  • Lock K, Janssen CR (2001) Zinc and cadmium burdens in terrestrial oligochaetes: use and significance in environmental risk assessment. Environ Toxicol Chem 20:2067–2072

    Article  CAS  Google Scholar 

  • Lock K, Janssen CR (2003) Comparative toxicity of a zinc salt, zinc powder and zinc oxide to Eisenia fetida, Enchytraeus albidus and Folsomia candida. Chemosphere 53:851–856

    Article  CAS  Google Scholar 

  • Ma H, Kabengi NJ, Bertsch PM, Unrine JM, Glenn TC, Williams PL (2011) Comparative phototoxicity of nanoparticle and bulk ZnO to a free-living nematode Caenorhabditis elegans: the importance of illumination mode and primary particle size. Environ Pollut 159:1473–1480

    Article  CAS  Google Scholar 

  • Ma H, Williams PL, Diamond SA (2013) Ecotoxicity of manufactured ZnO nanoparticles: a review. Environ Pollut 172:76–85

    Article  CAS  Google Scholar 

  • Manzo S, Rocco A, Carotenuto R, Picione FL, Miglietta ML, Rametta GF (2011) Investigation of ZnO nanoparticles’ ecotoxicological effects towards different soil organisms. Environ Sci Pollut Res 18:756–763

    Article  CAS  Google Scholar 

  • Maurer-Jones MA, Gunsolus IL, Murphy CJ, Haynes CL (2013) Toxicity of engineered nanoparticles in the environment. Anal Chem 85:3036–3049

    Article  CAS  Google Scholar 

  • Ministerio de Agricultura, Pesca y Alimentación (1994) Métodos oficiales de análisis: Tomo III. Secretaría General Técnica, Madrid, Spain

  • Muyssen BTA, Janssen CR (2001) Zinc acclimation and its effect on the zinc tolerance of Raphidocelis subcapitata and Chlorella vulgaris in laboratory experiments. Chemosphere 45:507–514

    Article  CAS  Google Scholar 

  • Organization for Economic Cooperation and Development (1984) Earthworm acute toxicity tests. OECD guidelines for the testing of chemicals. OECD, Paris

    Google Scholar 

  • Organization for Economic Cooperation and Development (2004) Daphnia sp. acute immobilization test. OECD guideline for testing of chemicals. OECD, Paris

    Google Scholar 

  • Organization for Economic Cooperation and Development (2006) Freshwater alga and cyanobacteria growth inhibition test. OECD guideline for testing of chemicals. Method 201. OECD, Paris

  • Pan B, Xing BS (2012) Applications and implications of manufactured nanoparticles in soils: a review. Eur J Soil Sci 63:437–456

    Article  CAS  Google Scholar 

  • Peralta-Videa JR, Zhao L, Lopez-Moreno ML, de la Rosa G, Hong J, Gardea-Torresdey JL (2011) Nanomaterials and the environment: a review for the biennium 2008–2010. J Hazard Mater 186:1–15

    Article  CAS  Google Scholar 

  • Pietrzak U, McPhail DC (2004) Copper accumulation distribution and fractionation in vineyard soils of Victoria Australia. Geoderma 122:151–166

    Article  CAS  Google Scholar 

  • Römkens PF, Guo H, Chu C, Liu T, Chiang C, Koopmans GF (2009) Characterization of soil heavy metal pools in paddy fields in Taiwan: chemical extraction and solid-solution partitioning. J Soil Sediment 9:216–228

    Article  Google Scholar 

  • Sbihi K, Cherifi O, El Gharmali A, Oudra B, Aziz F (2012) Accumulation and toxicological effects of cadmium, copper and zinc on the growth and photosynthesis of the freshwater diatom Planothidium lanceolatum (Brébisson) Lange-Bertalot: a laboratory study. J Mater Environ Sci 3:497–506

    CAS  Google Scholar 

  • Sizmur T, Palumbo-Roe B, Watts MJ, Hodson ME (2011) Impact of the earthworm Lumbricus terrestris (L.) on As, Cu, Pb and Zn mobility and speciation in contaminated soils. Environ Pollut 159:742–748

    Article  CAS  Google Scholar 

  • Smith BA, Egeler P, Gilgerg D, Hendershot W, Stephenson GL (2010) Uptake and elimination of cadmium and zinc by eisenia Andrei during exposure to low concentrations in artificial soil. Arch Environ Contam Toxicol 59:264–273

    Article  CAS  Google Scholar 

  • Tourinho PS, van-Gestel CAM, Lofts S, Svendsen C (2012) Metal based nanoparticles in soil: fate, behavior and effects on soil invertebrates. Environ Toxicol Chem 31:1679–1692

    Article  CAS  Google Scholar 

  • Trelo-ges V, Ruaysoongnern S, Chuasavathi (2002) Effect of earthworm activities (Pheretema sp.) on the changes in soil chemical properties at different soil depths of Nampong soil series (Ustoxic quartzipsamment) in Northeast Thailand. Pak J Biol Sci 5:32–35

    Article  Google Scholar 

  • Van-Straalen NM, Donker MH, Vijver MG, van-Gestel CA (2005) Bioavailability of contaminants estimated from uptake rates into soil invertebrates. Environ Pollut 136:409–417

    Article  CAS  Google Scholar 

  • Waalewijn-kool PL, Diez-Ortiz M, van-Gestel CAM (2012) Effect of different spiking procedures on the distribution and toxicity of ZnO nanoparticles in soil. Ecotoxicology 21:1797–1804

    Article  CAS  Google Scholar 

  • Wiench K, Wohlleben W, Hisgen V, Radke K, Salinas E, Zok S et al (2009) Acute and chronic effects of nano- and non-nano-scale TiO2 and ZnO particles on mobility and reproduction of the freshwater invertebrate Daphnia magna. Chemosphere 76:1356–1365

    Article  CAS  Google Scholar 

  • Zhao LJ, Peralta-Videa JR, Hernandez-Viezcas JA, Hong J, Gardea-Torresdey JL (2012) Transport and retention behavior of ZnO nanoparticles in two natural soils: effect of surface coating and soil composition. J Nano Red 17:229–242

    Article  CAS  Google Scholar 

  • Zhao L, Hernandez-Viezcas JA, Peralta-Videa JR, Bandyopadhyay S, Peng B, Munoz B et al (2013) ZnO nanoparticle fate in soil and zinc bioaccumulation in corn plants (Zea mays) influenced by alginate. Environ Sci Process Impacts 15:260

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Carmen del Rio and Jose Pareja for technical assistance. This research was funded by Spanish Projects RTA2010-00018-00-00 and EIADES S-2009/AMB/1478.

Author information

Authors and Affiliations

  1. Department of the Environment, INIA, Ctra A Coruña km 7.5, 28040, Madrid, Spain

    C. García-Gómez, M. Babin & M. D. Fernández

  2. Department of Chemistry and Agricultural Analysis, ETSI Agronomist (UPM), Ciudad Universitaria, 28040, Madrid, Spain

    A. Obrador & J. M. Álvarez

Authors
  1. C. García-Gómez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Babin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Obrador
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. M. Álvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. D. Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. García-Gómez.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

García-Gómez, C., Babin, M., Obrador, A. et al. Toxicity of ZnO Nanoparticles, ZnO Bulk, and ZnCl2 on Earthworms in a Spiked Natural Soil and Toxicological Effects of Leachates on Aquatic Organisms. Arch Environ Contam Toxicol 67, 465–473 (2014). https://doi.org/10.1007/s00244-014-0025-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-014-0025-7

Keywords

Search

Navigation