Environmental Monitoring and Assessment

, Volume 185, Issue 4, pp 3339–3348

Effects of aqueous suspensions of titanium dioxide nanoparticles on Artemia salina: assessment of nanoparticle aggregation, accumulation, and toxicity

  • Mehmet Ates
  • James Daniels
  • Zikri Arslan
  • Ibrahim O. Farah
Article

Abstract

Aquatic stability and impact of titanium dioxide nanoparticles (TiO2 NPs, 10–30 nm) were investigated using Artemia salina. Acute exposure was conducted on nauplii (larvae) and adults in seawater in a concentration range from 10 to 100 mg/L TiO2 NPs for 24 and 96 h. Rapid aggregation occurred in all suspensions of TiO2 NPs to form micrometer size particles. Yet, both nauplii and adults accumulated the aggregates significantly. Average TiO2 content in nauplii ranged from 0.47 to 3.19 and from 1.29 to 4.43 mg/g in 24 and 96 h, respectively. Accumulation in adults was higher ranging from 2.30 to 4.19 and from 4.38 to 6.20 mg/g in 24 and 96 h, respectively. Phase contrast microscopy images revealed that Artemia were unable to excrete the particles. Thus, the TiO2 aggregates filled inside the guts. No significant mortality or toxicity occurred within 24 h at any dose. Lipid peroxidation levels characterized with malondialdehyde concentrations were not statistically different from those of the controls (p > 0.05). These results suggested that suspensions of the TiO2 NPs were nontoxic to Artemia, most likely due to the formation of benign TiO2 aggregates in water. In contrast, both mortality and lipid peroxidation increased in extended exposure to 96 h. Highest mortality occurred in 100 mg/L TiO2 NP suspensions; 18 % for nauplii and 14 % for adults (LC50 > 100 mg/L). These effects were attributed to the particle loading inside the guts leading to oxidative stress as a result of impaired food uptake for a long period of time.

Keywords

TiO2 nanoparticle Artemia salina Aggregation Accumulation Toxicity 

References

  1. Adams, L. K., Lyon, D. Y., & Alvarez, P. J. J. (2006). Comparative ecotoxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Research, 40, 3527–3532.CrossRefGoogle Scholar
  2. Arslan, Z., Ertas, N., Tyson, J. F., Uden, P. C., & Denoyer, E. R. (2000). Determination of trace elements in marine plankton by inductively coupled plasma mass spectrometry (ICP-MS). Fresenius’ Journal of Analytical Chemistry, 366, 273–282.CrossRefGoogle Scholar
  3. Arslan, Z., Ates, M., McDuffy, W., Agachan, M. S., Farah, I. O., Yu, W. W., & Bednar, A. J. (2011). Probing metabolic stability of CdSe nanoparticles: alkaline extraction of free cadmium from liver and kidney samples of rats exposed to CdSe nanoparticles. Journal of Hazardous Materials, 192, 192–199.Google Scholar
  4. Bahnemann, D. W., Kholuiskaya, S. N., Dillert, R., Kulak, A. I., & Kokorin, A. I. (2002). Photodestruction of dichloroacetic acid catalyzed by nano-sized TiO2 particles. Applied Catalysis B: Environmental, 36, 161–169.CrossRefGoogle Scholar
  5. Benn, T. M., & Westerhoff, P. (2008). Nanoparticle silver released into water from commercially available sock fabrics. Environmental Science and Technology, 42, 4133–4139.CrossRefGoogle Scholar
  6. Chatterjee, R. (2008). The challenge of regulating nanomaterials. Environmental Science and Technology, 42, 339–343.CrossRefGoogle Scholar
  7. Choi, H., Stathatos, E., & Dionysiou, D. D. (2006). Sol–gel preparation of mesoporous photocatalytic TiO2 films and TiO2/Al2O3 composite membranes for environmental applications. Applied Catalysis B: Environmental, 63, 60–67.CrossRefGoogle Scholar
  8. Choi, J. Y., Ramachandran, G., & Kandlikar, M. (2009). The impact of toxicity testing costs on nanomaterial regulation. Environmental Science and Technology, 43, 3030–3034.CrossRefGoogle Scholar
  9. Farkas, J., Christian, P., Urrea, J. A., Roos, N., Hassellöv, M., Tollefsen, K. E., & Thomas, K. V. (2010). Effects of silver and gold nanoparticles on rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquatic Toxicology, 96, 44–52.CrossRefGoogle Scholar
  10. Farre, M., Gajda-Schrantz, K., Kantiani, L., & Barcelo, D. (2009). Ecotoxicity and analysis of nanomaterials in the aquatic environment. Analytical and Bioanalytical Chemistry, 393, 81–95.CrossRefGoogle Scholar
  11. Geranio, L., Heuberger, M., & Nowack, B. (2009). The behavior of silver nanotextiles during ecotoxicty and analysis of washing. Environmental Science and Technology, 43, 8113–8118.CrossRefGoogle Scholar
  12. Handy, R. D., Henry, T. B., Scown, T. M., Johnson, B. D., & Tyler, C. R. (2008). Manufactured nanoparticles: their uptake and effects on fish-a mechanistic analysis. Ecotoxicology, 17, 396–409.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. Hund-Rinke, K., & Simon, M. (2006). Ecotoxic effect of photocatalytic active nanoparticles (TiO2) on algae and daphnids. Environmental Science and Pollution Research, 13, 225–232.CrossRefGoogle Scholar
  15. Kanwar, A. (2007). Brine shrimp (Artemia salina) a marine animal for simple and rapid biological assays. Journal of Chinese Clinical Medicine, 2, 236–240.Google Scholar
  16. Kim, K. T., Klaine, S. J., Cho, J., Kim, S. H., & Kim, S. D. (2010). Oxidative stress responses of Daphnia magna exposed to TiO2 nanoparticles according to size fraction. Science of the Total Environment, 408, 2268–2272.CrossRefGoogle Scholar
  17. Lovern, S. B., & Klaper, R. (2006). Daphnia magna mortality when exposed to titanium dioxide and fullerene (C60) nanoparticles. Environmental Toxicology and Chemistry, 25, 1132–1137.CrossRefGoogle Scholar
  18. Mills, A., Lepre, A., Elliott, N., Bhopal, S., Parkin, I. P., & O’Neill, S. (2004). Characterization of the photocatalyst Pilkington Activ™: a reference film photocatalyst? Journal of Photochemistry and Photobiology A: Chemistry, 160, 213–224.CrossRefGoogle Scholar
  19. Moore, M. N. (2006). Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environment International, 32, 967–976.CrossRefGoogle Scholar
  20. Nunes, B. S., Carvalho, F. D., Guilhermino, L. M., & Van Stappen, G. (2006). Use of the genus Artemia in ecotoxicity testing. Environmental Pollution, 144, 453–462.CrossRefGoogle Scholar
  21. OECD. (2004). Organisation for Economic Co-operation and Development (OECD). Guideline for the Testing of Chemicals (Part 202).Google Scholar
  22. Pascual, P., Pedradas, J. R., Toribio, F., Lopez-Barea, J., & Peinado, J. (2003). Effect of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chemico-Biological Interactions, 145, 191–199.CrossRefGoogle Scholar
  23. Persoone, G., Van de Vell, A., Van Steertegem, M., & Nayer, B. (1989). Predictive value for laboratory tests with aquatic invertebrates: influence of experimental conditions. Aquatic Toxicology, 14, 149–166.CrossRefGoogle Scholar
  24. Sanchez, F., Sanz, F., Santa-Maria, A., Ros, J., De Vicente, M., Encinas, M., Vinagre, E., & Barahona, M. (1997). Acute sensitivity of three age classes of Artemia salina larvae to seven chlorinated solvents. Bulletin of Environmental Contamination and Toxicology, 59, 445–451.CrossRefGoogle Scholar
  25. Sayeed, I., Parvez, S., Pandey, S., Bin-Hafeez, B., & Raisuddin, S. (2003). Oxidative stress biomarkers of exposure to deltamethrin in freshwater fish, Channa punctatus Bloch. Ecotoxicology and Environmental Safety, 56, 295–301.CrossRefGoogle Scholar
  26. Schmidt, C. W. (2009). Nanotechnology-related environmental, health, and safety research examining the national strategy. Environmental Health Perspectives, 117, A158–A161.CrossRefGoogle Scholar
  27. Schulz, J., Hohenberg, H., Pflücker, F., Gärtner, E., Will, T., & Pfeiffer, S. (2002). Distribution of sunscreens on skin. Advanced Drug Delivery Reviews, 54, 157–163.CrossRefGoogle Scholar
  28. Sorgeloos, P. (1980). Availability of reference Artemia cysts. Marine Ecology Progress Series, 3, 363–364.CrossRefGoogle Scholar
  29. Van Ye, T. M., Roza, A. M., & Pieper, G. M. (1993). Inhibition of intestine lipid peroxidation does not minimize morphologic damage. Journal of Surgical Research, 55, 553–558.CrossRefGoogle Scholar
  30. Vanhaecke, P., Persoone, G., Claus, C., & Sorgeloos, P. (1981). Proposal for a short-term toxicity test with Artemia nauplii. Ecotoxicology and Environmental Safety, 5, 382–387.CrossRefGoogle Scholar
  31. Warheit, D. B., Hoke, R. A., Finlay, C., Donner, E. M., Reed, K. L., & Sayes, C. M. (2007). Development of a base set of toxicity tests using ultrafine TiO2 particles as a component of nanoparticle risk management. Toxicology Letters, 171, 99–110.CrossRefGoogle Scholar
  32. Wiench, K., Wohlleben, W., Hisgen, V., Radke, K., Salinas, E., Zok, S., & Landsiedel, R. (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.CrossRefGoogle Scholar
  33. Xiong, D., Fang, T., Yu, L., Sima, X., & Zhu, W. (2011). Effects of nano-scale TiO2, ZnO and their bulk counterparts on zebrafish: Acute toxicity, oxidative stress and oxidative damage. Science of the Total Environment, 409, 1444–1452.CrossRefGoogle Scholar
  34. Zeynalov, E. B., & Allen, N. S. (2006). Effect of micron and nano-grade titanium dioxides on the efficiency of hindered piperidine stabilizers in a model oxidative reaction. Polymer Degradation and Stability, 91, 931–939.CrossRefGoogle Scholar
  35. Zhao, J., Wang, Z., Liu, X., Xie, X., Zhang, K., & Xing, B. (2011). Distribution of CuO nanoparticles in juvenile carp (Cyprinus carpio) and their potential toxicity. Journal of Hazardous Materials, 197, 304–310.CrossRefGoogle Scholar
  36. Zhu, X., Zhu, L., Li, Y., Qi, R., Duan, Z., & Lang, Y. P. (2008). Comparative toxicity of several metal oxide nano-particle aqueous suspensions to zebrafish (Danio rerio) early developmental stage. Journal of Environmental Science and Health, Part A, 43, 278–284.CrossRefGoogle Scholar
  37. Zhu, X., Chang, Y., & Chen, Y. (2010). Toxicity and bioaccumulation of TiO2 nanoparticle aggregates in Daphnia magna. Chemosphere, 78, 209–215.CrossRefGoogle Scholar
  38. Zhu, X., Zhou, J., & Cai, Z. (2011). The toxicity and oxidative stress of TiO2 nanoparticles in marine abalone (Haliotis diversicolor supertexta). Marine Pollution Bulletin, 63, 334–338.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Mehmet Ates
    • 1
  • James Daniels
    • 1
  • Zikri Arslan
    • 1
  • Ibrahim O. Farah
    • 2
  1. 1.Department of Chemistry and BiochemistryJackson State UniversityJacksonUSA
  2. 2.Department of BiologyJackson State UniversityJacksonUSA

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