Effects of Zinc Oxide Nanoparticles on Panagrellus redivivus (Nematoda) and Folsomia candida (Collembola) in Various Test Media

  • Lola Virág Kiss
  • Krisztina Hrács
  • Péter István Nagy
  • Anikó Seres
Research paper


The toxic effects of zinc oxide (ZnO) nano- and non-nanoparticles on two species of soil organisms, the free-living nematode Panagrellus redivivus and the springtail Folsomia candida, were investigated. The toxicity of ZnO particles (with 15 and 140 nm average particle size) and ZnCl2 (used as a positive control for zinc ion dissolution) was tested in two different kinds of test media. Milli-Q water vs. soil solution was used for the tests involving P. redivivus, and plaster of paris vs. artificial soil for F. candida. For P. redivivus, application of the soil solution decreased the toxic effect. It is considered that this may be due to the less dissolved zinc ions, the organic matter content and ZnO aggregation. Furthermore, all of the compounds caused concentration-dependent mortality to the tested nematode species. In the tests with F. candida, the toxic effects of both ZnO and ZnCl2 were significantly lower in the tests involving plaster of paris. This could have resulted from the avoidance of the contaminated foods by the springtails. A decreasing effect on reproduction was observed only in the tests using artificial soil. Additionally, the ZnO particles of 140 nm significantly increased mortality in the soil solution test with P. redivivus and in the artificial soil in the tests with F. candida. Possibly, this is a consequence of a greater aggregation of the nanoparticle-sized ZnO at the end of the experiment, which resulted in a lower level of toxicity.


Nanomaterials Ecotoxicology Mortality test Reproduction test Test medium 



This study was supported by the National Young Talent Scholarship (NTP-NFTÖ-16-0588). We would like to express our thanks to Eötvös Loránd University, Central Research and Instrument Center for their help with scanning electron microscopy, Department of Chemistry at Szent István University for their help with inductively coupled plasma atomic emission spectroscopy and Department of Applied Chemistry at the University of Debrecen for their help in dynamic light scattering measurement. Special thanks are due to Professor Gábor Bakonyi for his advice.


  1. Adams LK, Lyon DY, Alvarez PJJ (2006) Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Res 40:3527–3532. CrossRefGoogle Scholar
  2. Ann LC, Mahmud S, Seeni A, Bakhori SKM, Sirelkhatim A, Mohamad D, Hasan H (2015) Structural morphology and in vitro toxicity studies of nano- and micro-sized zinc oxide structures. J Environ Chem Eng 3:436–444. CrossRefGoogle Scholar
  3. Bakonyi G, Seres A, Répási V, Juríková T, Szekeres L, Balla I (2009) Novel directions in the ecotoxicology involving soil animals. Állattani Közlemények 94:3–17Google Scholar
  4. Baruah S, Dutta J (2009) Nanotechnology applications in pollution sensing and degradation in agriculture: a review. Environ Chem Lett 7:191–204. CrossRefGoogle Scholar
  5. Bian SW, Mudunkotuwa IA, Rupasinghe T, Grassian VH (2011) Aggregation and dissolution of 4 nm ZnO nanoparticles in aqueous environments: influence of pH, ionic strength, size, and adsorption of humic acid. Langmuir 27:6059–6068. CrossRefGoogle Scholar
  6. Boyd W, Williams P (2003) Comparison of the sensitivity of three nematode species to copper and their utility in aquatic and soil toxicity tests. Environ Toxicol Chem 22:2768–2774CrossRefGoogle Scholar
  7. Chen H, Yada R (2011) Nanotechnologies in agriculture: new tools for sustainable development. Trends Food Sci Technol 22:585–594. CrossRefGoogle Scholar
  8. David CA, Galceran J, Rey-Castro C, Puy J, Companys E, Salvador J, Monne J, Wallace R, Vakourov A (2012) Dissolution kinetics and solubility of ZnO nanoparticles followed by AGNES. J Phys Chem 116:11758–11767Google Scholar
  9. Fountain MT, Hopkin SP (2001) Continuous monitoring of Folsomia candida (Insecta: Collembola) in a metal exposure test. Ecotoxicol Environ Saf 48:275–286. CrossRefGoogle Scholar
  10. Gange A (2000) Arbuscular mycorrhizal fungi, Collembola and plant growth. Trends Ecol Evol 15:369–372. CrossRefGoogle Scholar
  11. Jiang W, Mashayekhi H, Xing B (2009) Bacterial toxicity comparison between nano- and micro-scaled oxide particles. Environ Pollut 157:1619–1625. CrossRefGoogle Scholar
  12. Khare P, Sonane M, Pandey R, Ali S, Gupta KC, Satish A (2011) Adverse effects of TiO2 and ZnO nanoparticles in soil nematode, Caenorhabditis elegans. J Biomed Nanotechnol 7:116–117. CrossRefGoogle Scholar
  13. Khot LR, Sankaran S, Maja JM, Ehsani R, Schuster EW (2012) Applications of nanomaterials in agricultural production and crop protection: a review. Crop Prot 35:64–70. CrossRefGoogle Scholar
  14. Kiss LV, Hrács K, Nagy PI, Seres A (2015) Effects of ZnO with different particle size on terrestrial nematode and Collembolan test organisms. Állattani Közlemények 100:77–88. CrossRefGoogle Scholar
  15. Kiss LV, Hrács K, Nagy PI, Seres A (2016) Effects of nanoparticulated metal oxides on terrestrial microorganisms of special ecological importance—a review. Agrokémia És Talajt 65:115–134CrossRefGoogle Scholar
  16. 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. CrossRefGoogle Scholar
  17. Krogh PH (2008) Toxicity testing with the collembolans Folsomia fimetaria and Folsomia candida and the results of a ringtest. Miljøprojekt 66, DenmarkGoogle Scholar
  18. Li M, Pokhrel S, Jin X, Mädler L, Damoiseaux R, Hoek EMV (2011) Stability, bioavailability, and bacterial toxicity of ZnO and iron-doped ZnO nanoparticles in aquatic media. Environ Sci Technol 45:755–761. CrossRefGoogle Scholar
  19. Ma H, Kabengi NJ, Bertsch PM, Unrine JM, Glenn TC, Williams PL (2011) Comparative phototoxicity of nanoparticulate and bulk ZnO to a free-living nematode Caenorhabditis elegans: the importance of illumination mode and primary particle size. Environ Pollut 159:1473–1480. CrossRefGoogle Scholar
  20. Ma H, Williams PL, Diamond SA (2013) Ecotoxicity of manufactured ZnO nanoparticles. A review. Environ Pollut 172:76–85. CrossRefGoogle Scholar
  21. Manzo S, Rocco A, Carotenuto R, Picione FDL, Miglietta ML, Rametta G, Di Francia G (2011) Investigation of ZnO nanoparticles’ ecotoxicological effects towards different soil organisms. Environ Sci Pollut Res 18:756–763. CrossRefGoogle Scholar
  22. Miao AJ, Zhang XY, Luo Z, Chen CS, Chin WC, Santschi PH, Quigg A (2010) Zinc oxide-engineered nanoparticles: dissolution and toxicity to marine phytoplankton. Environ Toxicol Chem 29:2814–2822. CrossRefGoogle Scholar
  23. Moazezi N, Baghdadi M, Hickner MA, Moosavian MA (2018) Modeling and Experimental Evaluation of Ni(II) and Pb(II) Sorption from Aqueous Solutions Using a Polyaniline/CoFeC6N6 Nanocomposite. J Chem Eng Data 6:741–750. CrossRefGoogle Scholar
  24. Petersen EJ (2015) Control experiments to avoid artifacts and misinterpretations in nanoecotoxicology testing. NIST Spec Publ 1200–11:1–7. Google Scholar
  25. Pipan-Tkalec Z, Drobne D, Jemec A, Romih T, Zidar P, Bele M (2010) Zinc bioaccumulation in a terrestrial invertebrate fed a diet treated with particulate ZnO or ZnCl2 solution. Toxicology 269:198–203. CrossRefGoogle Scholar
  26. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0Google Scholar
  27. Samoiloff MR (1987) Nematodes as indicators of toxic environmental contaminants. In: Veech JA, Dickson DW (eds) Vistas on Nematology. Society of Nematologists, Lakeland, pp 433–439Google Scholar
  28. Samoiloff MR, Schulz S, Jordan Y, Denich K, Arnott E (1980) A rapid simple long-term toxicity assay for aquatic contaminants using the nematode Panagrellus redivivus. Can J Fish Aquat Sci 37:1167–1174CrossRefGoogle Scholar
  29. Sávoly Z, Nagy P, Havancsák K, Záray G (2012) Microanalytical investigation of nematodes. Microchem J 105:83–87. CrossRefGoogle Scholar
  30. Sávoly Z, Hrács K, Oemmer B, Streli C, Záray G, Nagy PI (2016) Uptake and toxicity of nano-ZnO in the plant-feeding nematode, Xiphinema vuittenezi: the role of dissolved zinc and nanoparticle-specific effects. Environ Sci Pollut Res 23:9669–9678. CrossRefGoogle Scholar
  31. Sirelkhatim A, Mahmud S, Seeni A, Kaus NHM, Ann LC, Bakhori SKM, Hasan H, Dasmawati M (2015) Review on zinc oxide nanoparticles: antibacterial activity and toxicity mechanism. Nano-Micro Lett 7:219–242. CrossRefGoogle Scholar
  32. Sommer RJ (2005) Evolution of development in nematodes related to C. elegans. In: WormBook (Ed.) The C. elegans research community. WormBook (the online review of C. elegans biology), Germany, pp 1–17.
  33. Srinivasan J, Dillman AR, Macchietto MG, Heikkinen L, Lakso M, Fracchia KM, Antoshechkin I, Mortazavi A, Wong G, Sternberg PW (2013) The draft genome and transcriptome of Panagrellus redivivus are shaped by the harsh demands of a free-living lifestyle. Genetics 193:1279–1295. CrossRefGoogle Scholar
  34. Stankovic´ A, Dimitrijevic´ S, Uskokovic´ D (2013) Influence of size scale and morphology on antibacterial properties of ZnO powders hydrothermally synthesized using different surface stabilizing agents. Colloids Surf B Biointerfaces 102:21–28CrossRefGoogle Scholar
  35. Sternberg PW, Horvitz HR (1982) Postembryonic nongonadal cell lineages of the nematode Panagrellus redivivus: description and comparison with those of Caenorhabditis elegans. Dev Biol 205:181–205CrossRefGoogle Scholar
  36. Talebian N, Amininezhad SM, Doudi M (2013) Controllable synthesis of ZnO nanoparticles and their morphology-dependent antibacterial and optical properties. J Photochem Photobiol B Biol 120:66–73. CrossRefGoogle Scholar
  37. Tong T, Shereef A, Wu J, Binh CTT, Kelly JJ, Gaillard J-F, Gray KA (2013) Effects of material morphology on the phototoxicity of nano-TiO2 to bacteria. Environ Sci Technol 47:12486–12495. CrossRefGoogle Scholar
  38. Tourinho PS, Van Gestel CAM, Lofts S, Svendsen C, Soares AMVM, Loureiro S (2012) Metal-based nanoparticles in soil: fate, behavior, and effects on soil invertebrates. Environ Toxicol Chem 31:1679–1692. CrossRefGoogle Scholar
  39. TOXRATLIGHT2.08 (n.d.) Software for statistical evaluation of biotests in ecotoxicology. ToxRat Solutions GmbH, Germany, Alsdorf. ToxRat Solutions GmbH, Germany, AlsdorfGoogle Scholar
  40. 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. CrossRefGoogle Scholar
  41. Waalewijn-Kool PL, Diez Ortiz M, Van Straalen NM, Van Gestel CAM (2013) Sorption, dissolution and pH determine the long-term equilibration and toxicity of coated and uncoated ZnO nanoparticles in soil. Environ Pollut 178:59–64. CrossRefGoogle Scholar
  42. Waalewijn-Kool PL, Rupp S, Lofts S, Svendsen C, van Gestel CAM (2014) Effect of soil organic matter content and pH on the toxicity of ZnO nanoparticles to Folsomia candida. Ecotoxicol Environ Saf 108:9–15. CrossRefGoogle Scholar
  43. Wah Chu K, Chow KL (2002) Synergistic toxicity of multiple heavy metals is revealed by a biological assay using a nematode and its transgenic derivative. Aquat Toxicol 61:53–64. CrossRefGoogle Scholar
  44. Wang H, Wick RL, Xing B (2009) Toxicity of nanoparticulate and bulk ZnO, Al2O3 and TiO2 to the nematode Caenorhabditis elegans. Environ Pollut 157:1171–1177. CrossRefGoogle Scholar
  45. Wu Q, Wang W, Li Y, Li Y, Ye B, Tang M, Wang D (2012) Small sizes of TiO2-NPs exhibit adverse effects at predicted environmental relevant concentrations on nematodes in a modified chronic toxicity assay system. J Hazard Mater 243:161–168. CrossRefGoogle Scholar

Copyright information

© University of Tehran 2018

Authors and Affiliations

  1. 1.Department of Zoology and Animal EcologySzent István UniversityGödöllőHungary

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