The impact of nanoparticles on fish health is still a matter of debate, since nanotechnology is quite recent. In this study, freshwater benthonic juvenile fish Prochilodus lineatus were exposed through water to three concentrations of TiO2 (0.1, 1, and 10 μg l−1) and ZnO (7, 70, and 700 μg l−1) nanoparticles, as well as to a mixture of both (TiO2 1 μg l−1 + ZnO 70 μg l−1) for 5 and 30 days. Nanoparticle characterization revealed an increase of aggregate size in the function of concentration, but suspensions were generally stable. Fish mortality was high at subchronic exposure to 70 and 700 μg l−1 of ZnO. Nanoparticle exposure led to decreased acetylcholinesterase activity either in the muscle or in the brain, depending on particle composition (muscle—TiO2 10 μg l−1; brain—ZnO 7 and 700 μg l−1), and protein oxidative damage increased in the brain (ZnO 70 μg l−1) and gills (ZnO 70 μg l−1 and mixture) but not in the liver. Exposed fish had more frequent alterations in the liver (necrosis, vascular congestion, leukocyte infiltration, and basophilic foci) and gills (hyperplasia and epithelial damages, e.g., epithelial disorganization and epithelial loss) than the control fish. Thus, predicted concentrations of TiO2 and ZnO nanoparticles caused detectable effects on P. lineatus that may have important consequences to fish health. But, these effects are much more subtle than those usually reported in the scientific literature for high concentrations or doses of metal nanoparticles.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Andersson-Willman B, Gehrmann U, Cansu Z, Buerki-Thurnherr T, Krug HF, Gabrielsson S, Scheynius A (2012) Effects of subtoxic concentrations of TiO2 and ZnO nanoparticles on human lymphocytes, dendritic cells and exosome production. Toxicol Appl Pharmacol 264:94–103
Ates M, Daniels J, Arslan Z, Farah Ibrahim O (2013) Effects of aqueous suspensions of titanium dioxide nanoparticles on Artemia salina: assessment of nanoparticle aggregation, accumulation, and toxicity. Environ Monit Assess 3339:48–185
Baun A, Hartmann NB, Grieger K, Kusk KO (2008) Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing. Ecotoxicol 17:387–395
Boyle D, Al-Bairuty GA, Ramsden CS, Sloman KA, Henry TB, Handy RD (2013) Subtle alterations in swimming speed distributions of rainbow trout exposed to titanium dioxide nanoparticles are associated with gill rather than brain injury. Aquat Toxicol 126:116–127
Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254
Čolović MB, Krstić DZ, Lazarević-Pašti TD, Bondžić AM, Vasić VM (2013) Acetylcholinesterase inhibitors. Pharmacol Toxicol 11(3):315–335
Cuña RHD, Rey GV, Piol MN, Guerrero NV, Maggese MC, Lo Nostro FL (2011) Assessment of the acute toxicity of the organochlorine pesticide endosulfan in Cichlasoma dimerus (Teleostei, Perciformes). Ecotoxicol Environ Saf 4:1065–1073
Ellmann GL, Coutney KO, Andres V, Featherstone RMA (1961) New and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
Federici G, Shaw BJ, Handy RD (2007) Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 84:415–430
Garcia-Santos S, Monteiro SM, Carrola J, Fontainhas Fernandes A (2007) Alterações histológicas em brânquias de tilápia nilotica Oreochromis niloticus causadas pelo cádmio. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 59:376–38
Gheshlaghi ZN, Riazi GH, Ahmadian S, Ghafari M, Mahinpour R (2008) Toxicity and interaction of titanium dioxide nanoparticles with microtubule protein. Acta Biochim Biophys Hung 40:777–782
Gornati R, Palpis E, Gioacchino MDi (2009) In vivo and in vitro models for nanotoxicology testing. In: S. C. Sahu; D. A. Casciano (Eds.); Nanotoxicity—from in vitro and in vivo models to health risks 610
Griffitt RJ, Weil R, Hyndman KA, Denslow ND, Powers K, Taylor D (2007) Exposure to copper nanoparticles causes gill injury and acute lethality in zebrafish (Danio rerio). Environ Sci Technol 41:8178–8186
Hao L, Wang Z, Xing B (2009) Effect of sub-acute exposure to TiO2 nanoparticles on oxidative stress and histopathological changes in juvenile carp (Cyprinus carpio). J Environ Sci 21:1459–1466
Hao L, Chen L, Hao J, Zhong N (2013) Bioaccumulation and sub-acute toxicity of zinc oxide nanoparticles in juvenile carp (Cyprinus carpio): a comparative study with its bulk counterparts. Ecotoxicol Environ Saf 91:52–60
Hoyt VW, Mason E (2008) Nanotechnology emerging health issues. J Chem Health Saf 15:10–15
Jiang ZY, Woollard ACS, Wolff SP (1991) Lipid hydroperoxides measurement by oxidation of Fe2+ in the presence of xylenol orange. Comparison with the TBA assay and an iodometric method. Lipids 26:853–856
Levine RL, Williams JA, Stadtman EP, Schacter E (1994) Carbonyl assays for determination of oxidativiley modified proteins. Methods Enzimol 233:246–257
Li N, Xia T, Nel AE (2008) The role of oxidative stress in ambient particulate matter-induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radic Biol Med 44:1689–1699
Malvern Instruments (2005) Zetasizer Nano Series user manual. Worcestershire-UK. Issue 2.2
Mela M, Randi MF, Ventura DF, Carvalho CEV, Pelletier E, Oliveira Ribeiro C (2007) Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias malabaricus. Ecotoxicol Environ Saf 68:426–435
Mela M, Guiloski IC, Doria HB, Randi MAF, Oliveira Ribeiro C, Pereira L, Maraschi AC, Prodocimo V, Freire CA, Silva de Assis HC (2013) Effects of the herbicide atrazine in neotropical catfish (Rhamdia quelen). Ecotoxicol Environ Saf 93:13–21
Misra SK, Dybowska A, Berhanu D, Luoma S, Valsemi-Jones E (2012) The complexity of nanoparticle dissolution and its importance in nanotoxicological studies. Sci Total Environ 438:225–232
Moura-Costa DD, Filipak Neto F, Costa MDM, Morais RN, Garcia JRE, Esquivel BM, Oliveira-Ribeiro CA (2010) Vitellogenesis and other physiological responses induced by 17-beta-estradiol in males of freshwater fish Rhamdia quelen. Comp Biochem Physiol C 151:248–257
Mueller NC, Nowack B (2008) Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–4453
Murphy SD (1986) Pesticides. The basic science of poisons. Macmillan, NY, pp 519–581
Nel A, Xia T, Madler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 31:622–627
Pérez S, Farré M, Barceló D (2009) Analysis, behavior and ecotoxicity of carbon-based nanomaterials in the aquatic environment. TrAC Trends Anal Chem 28:820–832
Quinlan GJ, Gutteridge JMC (2000) Carbonyl assay for oxidative damage to proteins. In: Taniguchi N, Gutteridge JMC (eds) Experimental protocols for reactive oxygen and nitrogen species. Oxford University, New York, pp 257–258
Schilling K, Bradford B, Castelli D, Dufour E, Nash FJ, Pape W, Schulte S, Tooley I, Van Den Bosch J, Schellauf F (2010) Human safety review of “nano” titanium dioxide and zinc oxide. Photochem Photobiol Sci 9:495–509
Sedlak J, Lindsay RH (1968) Estimation of total protein bound and nonprotein sulphydril groups in tissues with Ellman’s reagent. Anal Biochem 25:192–205
Singh S, Shi T, Duffin R et al (2007) Endocytosis, oxidative stress and IL-8 expression in human lung epithelial cells upon treatment with fine and ultrafine TiO2: role of the specific surface area and of surface methylation of the particles. Toxicol Appl Pharmacol 222:141–151
Westerhoff P, Nowack B (2013) Searching for global descriptors of engineered nanomaterial fate and transport in the environment. Acc Chem Res 46(3):844–853
Xia J, Zhao HZ, Lu GH (2013) Effects of selected metal oxide nanoparticles on multiple biomarkers in Carassius auratus. Biomed Environ Sci 9:742–749
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. Sci Total Environ 409:1444–1452
Zhao X, Wang S, Wu Y, You H, Lv L (2013) Acute ZnO nanoparticles exposure induces developmental toxicity, oxidative stress and DNA damage in embryo-larval zebrafish. Aquat Toxicol 137:49–59
Zhu X, Wang J, Zhang X, Chang Y, Chen Y (2009) The impact of ZnO nanoparticle aggregates on the embryonic development of zebrafish (Danio rerio). Nanotechnology 20:195103 (9pp)
This research was supported by Fundação Araucária (financial support, protocol 17843) and CAPES (Ms scholarship). The authors acknowledge the Electron Microscopy Center of the Federal University of Paraná for the technical support.
Conflict of interest
The authors declare that they have no competing interests.
R. R. Miranda and F. Filipak Neto contributed equally to this work.
Responsible editor: Henner Hollert
About this article
Cite this article
Miranda, R.R., Damaso da Silveira, A.L.R., de Jesus, I.P. et al. Effects of realistic concentrations of TiO2 and ZnO nanoparticles in Prochilodus lineatus juvenile fish. Environ Sci Pollut Res 23, 5179–5188 (2016). https://doi.org/10.1007/s11356-015-5732-8
- Metal oxide nanoparticle
- Oxidative stress