Environmental Science and Pollution Research

, Volume 20, Issue 5, pp 3456–3463 | Cite as

Toxicity of two types of silver nanoparticles to aquatic crustaceans Daphnia magna and Thamnocephalus platyurus

  • Irina Blinova
  • Jukka Niskanen
  • Paula Kajankari
  • Liina Kanarbik
  • Aleksandr Käkinen
  • Heikki Tenhu
  • Olli-Pekka Penttinen
  • Anne Kahru
Research Article


Although silver nanoparticles (NPs) are increasingly used in various consumer products and produced in industrial scale, information on harmful effects of nanosilver to environmentally relevant organisms is still scarce. This paper studies the adverse effects of silver NPs to two aquatic crustaceans, Daphnia magna and Thamnocephalus platyurus. For that, silver NPs were synthesized where Ag is covalently attached to poly(vinylpyrrolidone) (PVP). In parallel, the toxicity of collargol (protein-coated nanosilver) and AgNO3 was analyzed. Both types of silver NPs were highly toxic to both crustaceans: the EC50 values in artificial freshwater were 15–17 ppb for D. magna and 20–27 ppb for T. platyurus. The natural water (five different waters with dissolved organic carbon from 5 to 35 mg C/L were studied) mitigated the toxic effect of studied silver compounds up to 8-fold compared with artificial freshwater. The toxicity of silver NPs in all test media was up to 10-fold lower than that of soluble silver salt, AgNO3. The pattern of the toxic response of both crustacean species to the silver compounds was almost similar in artificial freshwater and in natural waters. The chronic 21-day toxicity of silver NPs to D. magna in natural water was at the part-per-billion level, and adult mortality was more sensitive toxicity test endpoint than the reproduction (the number of offspring per adult).


Ecotoxicology Crustaceans Silver nanoparticles Collargol Bioavailability Natural water 



This study was supported by the Estonian Science Foundation Projects ETF8066, ETF8561, and EU Central Baltic INTERREG IVA programme 2007–2013 project: Risk Management and Remediation of Chemical Accidents (RIMA). Julien Pinaton is acknowledged for participation in the synthesis of PVP-grafted silver nanoparticles and Prof. Damjana Drobne (University of Ljubljana) for the TEM image of collargol.

Supplementary material

11356_2012_1290_MOESM1_ESM.docx (1.4 mb)
ESM 1 (DOCX 1,440 kb)


  1. Allen HJ, Impellitteri CA, Macke DA, Heckman JL, Poynton HC, Lazorchak JM, Govindaswamy S, Roose DL, Nadagouda MN (2010) Effects from filtration, capping agents, and presence/absence of food on the toxicity of silver nanoparticles to Daphnia magna. Environ Toxicol Chem 29:2742–2750CrossRefGoogle Scholar
  2. Bianchini A, Wood CM (2008) Does sulfide or water hardness protect against chronic silver toxicity in Daphnia magna? A critical assessment of the acute-to-chronic toxicity ratio for silver. Ecotoxicol Environ Safe 71:32–40CrossRefGoogle Scholar
  3. Blinova I, Ivask A, Heinlaan M, Mortimer M, Kahru A (2010) Ecotoxicity of nanoparticles of CuO and ZnO in natural water. Environ Pollut 158:41–47CrossRefGoogle Scholar
  4. Bone AJ, Colman BP, Gondikas AP, Newton KM, Harrold KH, Cory RM, Unrine JM, Klaine SJ, Matson CW, Di Giulio RT (2012) Biotic and abiotic interactions in aquatic microcosms determine fate and toxicity of ag nanoparticles: part 2-toxicity and Ag speciation. Environ Sci Technol 46:6925–6933CrossRefGoogle Scholar
  5. Chiefari J, Chong YK, Ercole F, Krstina J, Jeffery J, Le TPT, Mayadunne RTA, Meijs GF, Moad CL, Moad G, Rizzardo E, Thang SH (1998) Living free-radical polymerization by reversible addition–fragmentation chain transfer: the RAFT process. Macromolecules 31:5559–5562CrossRefGoogle Scholar
  6. Erickson RJ, Brooke LT, Kahl MD, Vende Venter F, Harting SL, Markee TP, Spehar RL (1998) Effects of laboratory test conditions on the toxicity of silver to aquatic organisms. Environ Toxicol Chem 17:572–578CrossRefGoogle Scholar
  7. Fabrega J, Fawcett S, Renshaw J, Lead J (2009) Silver nanoparticle impact on bacterial growth: effect of pH, concentration, and organic matter. Environ Sci Technol 43:7285–7290CrossRefGoogle Scholar
  8. Fabrega J, Luoma SN, Tyler CR, Galloway TS, Lead JR (2011) Silver nanoparticles: behaviour and effects in the aquatic environment. Environ Int 37:517–531CrossRefGoogle Scholar
  9. Fung MC, Bowen D (1996) Silver products for medical indications: risk-benefit assessment. J Toxicol Clin Toxicol 34:119–126CrossRefGoogle Scholar
  10. Gao J, Youn S, Hovsepyan A, Llaneza V, Bitton G, Bonzongo JC (2009) Dispersion and toxicity of selected manufactured nanomaterials in natural river water samples: effects of water chemical composition. Environ Sci Technol 43:3322–3328CrossRefGoogle Scholar
  11. Goddard D, Gruber J (1999) Principles of polymer science and technology in cosmetics and personal care. Marcel Dekker, Inc., New YorkCrossRefGoogle Scholar
  12. Greulich C, Diendorf J, Simon T, Eggeler G, Epple M, Köller M (2011) Uptake and intracellular distribution of silver nanoparticles in human mesenchymal stem cells. Acta Biomater 7:347–354CrossRefGoogle Scholar
  13. Griffitt RJ, Luo J, Gao J, Bonzongo JC, Barber DS (2008) Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem 27:1972–1978CrossRefGoogle Scholar
  14. Haaf F, Sanner A, Straub F (1985) Water soluble, curable copolymers, methods of preparation and uses thereof. Polym J 17:143–152CrossRefGoogle Scholar
  15. Kahru A, Dubourguier HC (2010) From ecotoxicology to nanoecotoxicology. Toxicology 269:105–119CrossRefGoogle Scholar
  16. Koukal B, Rosse P, Reinhardt A, Ferrari B, Wilkinson J, Loizeau J-L, Dominik J (2007) Effect of Pseudokirchneriella subcapitata (Chlorophyceae) exudates on metal toxicity and colloid aggregation. Water Res 41:63–70CrossRefGoogle Scholar
  17. Kuo TT, Hu S, Huang CL, Chan HL, Chang MJW, Dunn P, Chen YJ (1997) Cutaneous involvement in polyvinylpyrrolidone storage disease: a clinicopathologic study of five patients, including two patients with severe anemia. Am J Surg Pathol 21:1361–1367CrossRefGoogle Scholar
  18. Ledwith DM, Whelan AM, Kelly JM (2007) A rapid, straight-forward method for controlling the morphology of stable silver nanoparticles. Mater J Chem 17:2459–2464CrossRefGoogle Scholar
  19. List of manufactured nanomaterials and list of endpoints for phase one of the sponsorship programme for the testing of manufactured nanomaterials: revision. (2010) OECD, ENV/JM/MONO. At Accessed May 2012.
  20. Liu J, Hurt RH (2010) Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ Sci Technol 44:2169–2175CrossRefGoogle Scholar
  21. Lowe AB, Sumerlin BS, Donovan MS, McCormick CL (2002) Facile preparation of transition metal nanoparticles stabilized by well-defined (co)polymers synthesized via aqueous reversible addition-fragmentation chain transfer polymerization. J Am Chem Soc 124:11562–11563CrossRefGoogle Scholar
  22. Mueller NC, Nowack B (2008) Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–4453CrossRefGoogle Scholar
  23. Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ, Quigg A, Santschi PH, Sigg L (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants and fungi. Ecotoxicology 17:372–386CrossRefGoogle Scholar
  24. Nebeker AV, McAuliffe CK, Mshar R, Stevens DG (1983) Toxicity of silver to steelhead and rainbow trout, fathead minnows and Daphnia magna. Environ Toxicol Chem 2:95–104Google Scholar
  25. Niskanen J, Shan J, Tenhu H, Jiang H, Kauppinen E, Barranco V, Picó F, Yliniemi K, Kontturi K (2010) Synthesis of copolymer-stabilized silver nanoparticles for coating materials. Colloid Polym Sci 288:543–553CrossRefGoogle Scholar
  26. Nowack B, Krug H, Height M (2011) 120 years of nanosilver history: implications for policy makers. Environ Sci Technol 45:1177–1183CrossRefGoogle Scholar
  27. Ratte HT (1999) Bioaccumulation and toxicity of Ag compounds: a review. Environ Toxicol Chem 18:89–108CrossRefGoogle Scholar
  28. Shan J, Nuopponen M, Jiang H, Kauppinen E, Tenhu H (2003) Preparation of poly (N-isopropylacrylamide)—monolayer-protected gold clusters: synthesis methods, core size, and thickness of monolayer. Macromolecules 36:4526–4533CrossRefGoogle Scholar
  29. Tolaymat TM, Badawy AM, Genaidy A, Scheckel KG, Luxton TP, Suidan M (2010) An evidence-based environmental perspective of manufactured silver nanoparticle in syntheses and applications: a systematic review and critical appraisal of peer-reviewed scientific papers. Sci Total Environ 408:999–1006CrossRefGoogle Scholar
  30. Unrine JM, Colman BP, Bone AJ, Gondikas AP, Matson CW (2012) Biotic and abiotic interactions in aquatic microcosms determine fate and toxicity of Ag nanoparticles: part 1—aggregation and dissolution. Environ Sci Technol 46:6915–6924CrossRefGoogle Scholar
  31. US EPA (2005) Standard methods for examination of water and wastewater. At Accessed March 2012
  32. Weinberg H, Galyean A, Leopold M (2011) Evaluating engineered nanoparticles in natural waters. Trend Anal Chem 30:72–83CrossRefGoogle Scholar
  33. Wijnhoven SWP, Peijnenburg WJGM, Herberts CA, Hagens WI, Oomen AG, Heugens EHW, Roszek B, Bisschops J, Gosens I, Van De Meent D, Dekkers S, De Jong WH, Van Zijverden M, Sips AJAM, Geertsma RE (2009) Nano-silver: a review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology 3:109–138CrossRefGoogle Scholar
  34. Woodrow Wilson Database (2012) At Accessed March 2011
  35. Xia T, Zhao Y, Sager T, George S, Pokhrel S, Li N, Schoenfeld D, Meng H, Lin S, Wang X, Wang M, Ji Z, Zink JI, Mädler L, Castranova V, Lin S, Nel AE (2011) Decreased dissolution of ZnO by iron doping yields nanoparticles with reduced toxicity in the rodent lung and zebrafish embryos. ACS Nano 5:1223–1235CrossRefGoogle Scholar
  36. Zhao CM, Wang WX (2010) Biokinetic uptake and efflux of silver nanoparticles in Daphnia magna. Environ Sci Technol 44:7699–7704CrossRefGoogle Scholar
  37. Zhao CM, Wang WX (2011) Comparison of acute and chronic toxicity of silver nanoparticles and silver nitrate to Daphnia magna. Environ Toxicol Chem 30:885–892CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Irina Blinova
    • 1
  • Jukka Niskanen
    • 2
  • Paula Kajankari
    • 3
  • Liina Kanarbik
    • 1
    • 4
  • Aleksandr Käkinen
    • 1
    • 4
  • Heikki Tenhu
    • 2
  • Olli-Pekka Penttinen
    • 3
  • Anne Kahru
    • 1
  1. 1.Laboratory of Molecular GeneticsNational Institute of Chemical Physics and BiophysicsTallinnEstonia
  2. 2.Laboratory of Polymer Chemistry, Department of ChemistryUniversity of HelsinkiHelsinkiFinland
  3. 3.Department of Environmental SciencesUniversity of HelsinkiLahtiFinland
  4. 4.Department of Chemical and Materials TechnologyTallinn University of TechnologyTallinnEstonia

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