Cited by 208Environmental Toxicology and EcotoxicologyNanoparticles: synthesis and applicationsMicroplastics and Plastic Pollution

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Biological Surface Coating and Molting Inhibition as Mechanisms of TiO2 Nanoparticle Toxicity in Daphnia magna

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Dabrunz, André, Duester, Lars, Prasse, Carsten, Seitz, Frank, Rosenfeldt, Ricki, Schilde, Carsten, Schaumann, Gabriele E., Schulz, Ralf·2011·PLoS ONE

DOI 10.1371/journal.pone.0020112PMC PMC3103543

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Abstract

The production and use of nanoparticles (NP) has steadily increased within the last decade; however, knowledge about risks of NP to human health and ecosystems is still scarce. Common knowledge concerning NP effects on freshwater organisms is largely limited to standard short-term (≤48 h) toxicity tests, which lack both NP fate characterization and an understanding of the mechanisms underlying toxicity. Employing slightly longer exposure times (72 to 96 h), we found that suspensions of nanosized (∼100 nm initial mean diameter) titanium dioxide (nTiO(2)) led to toxicity in Daphnia magna at nominal concentrations of 3.8 (72-h EC(50)) and 0.73 mg/L (96-h EC(50)). However, nTiO(2) disappeared quickly from the ISO-medium water phase, resulting in toxicity levels as low as 0.24 mg/L (96-h EC(50)) based on measured concentrations. Moreover, we showed that nTiO(2) (∼100 nm) is significantly more toxic than non-nanosized TiO(2) (∼200 nm) prepared from the same stock suspension. Most importantly, we hypothesized a mechanistic chain of events for nTiO(2) toxicity in D. magna that involves the coating of the organism surface with nTiO(2) combined with a molting disruption. Neonate D. magna (≤6 h) exposed to 2 mg/L nTiO(2) exhibited a "biological surface coating" that disappeared within 36 h, during which the first molting was successfully managed by 100% of the exposed organisms. Continued exposure up to 96 h led to a renewed formation of the surface coating and significantly reduced the molting rate to 10%, resulting in 90% mortality. Because coating of aquatic organisms by manmade NP might be ubiquitous in nature, this form of physical NP toxicity might result in widespread negative impacts on environmental health.

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Figure 1 Mean immobilization (±SD; n = 6) of D. magna exposed to 2 mg/L TiO2 of different sizes. White bars: ∼200 nm TiO2; grey bars: ∼100 nm nTiO2.CC BY · PubMed Central

Figure 2 Mean immobilization (±SD; n = 6) of daphnids after 72 and 96 h of exposure to nominal concentrations of 0, 0.5, 1, 2, 4 and 8 mg nTiO2 (∼100 nm).CC BY · PubMed Central

Figure 3 Dissipation of nTiO2 (∼100 nm) from the water phase. nTiO2 was measured as 47Ti, at initial concentrations of 0.5, 1, 2, 4, and 8 mg/L nTiO2 (ISO medium; means ± SD; n = 3).CC BY · PubMed Central

Figure 4 Development of biological surface coating in a 96-h toxicity test at 2 mg/L nTiO2 in ISO-medium. (A) 24 h, before 1st molting; (B) 25 h, about 1 h after 1st molting with arrow indicating renewed particle adhesions at filtration apparatus and the lower ventral gap; (C) 48 h; (D) 72 h; (E) 96 h; (F) ESEM-EDX picture of nTiO2 particle agglomerates colored in red on spine of D. magna following 48 h of exposure to, nTiO2 particles at 2 mg/L.CC BY · PubMed Central

Figure 5 Molting success of juvenile D. magna (age ≤6 at 0 h) exposed to 2 mg/L nTiO2 (∼100 nm). Bars between 24 and 48 h on the left indicate the percentage of individuals passing the first molting, bars on the right, from 66 h onwards, represent those individuals passing the second molting. Black dots indicate the percentage of immobilized D. magna in the nTiO2 treatment.CC BY · PubMed Central

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“…relationship data on D. magna immobilization were retrieved from 20 reports: Briffa et al. (2018), Cui et al. (2017), Cupi et al. (2016), Dabrunz et al. (2011), Heinlaan et al. (2008), Kim et al. (2017), Lee et al. (2012), Ma et al. (2012), Newton et al. (2013), Oleszczuk et al.…”
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No chronic effects on biochemical biomarkers, feeding and survival of carnolian honeybees (Apis mellifera carnica) after exposure to nanosized carbon black and titanium dioxide
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“toxicity responses of exposed organisms (Dabrunz et al. 2011; Warheit et al. 2007).”
BackgroundInfluential
A holistic NMR framework to understand environmental impact: Examining the impacts of superparamagnetic iron oxide nanoparticles (SPIONs) in Daphnia magna via imaging, spectroscopy, and metabolomics
Jenne, A., Soong, R., Gruschke, O. G., Bastawrous, M., Monks, P., Moloney, C., Brougham, D. F., Busse, F., Bermel, W., Courtier‐Murias, D., et al. (2022) · Magnetic Resonance in Chemistry · doi:10.1002/mrc.5315 · Cited by 7
Oxidized Carbo-Iron causes reduced reproduction and lower tolerance of juveniles in the amphipod Hyalella azteca
Weil, M., Meißner, T., Springer, A., Bundschuh, M., Hübler, L., Schulz, R., & Duis, K. (2016) · Aquatic Toxicology · doi:10.1016/j.aquatox.2016.10.028 · Cited by 7
Aquatische Ökotoxizität von Nanopartikeln – Versuche zur Aufklärung von Nanopartikeleffekten
Skjolding, L. M., Sørensen, S. N., Hartmann, N. B., Hjorth, R., Hansen, S. F., & Baun, A. (2016) · Angewandte Chemie · doi:10.1002/ange.201604964 · Cited by 7
Miniaturizing Nanotoxicity Assays in Daphnids
Kakavas, D., Panagiotidis, K., Rochfort, K. D., & Grintzalis, K. (2024) · Animals · doi:10.3390/ani14142046 · Cited by 6
Antiparasitic effect of biogenic iron nanoparticles against the fish ectoparasite Argulus siamensis: In vitro study
Brahmchari, R. K., Kumari, P., Kumar, S., Sharma, R., Prasad, K. P., Srivastava, P., & Raman, R. P. (2023) · Indian Journal of Fisheries · doi:10.21077/ijf.2023.70.3.132524-14 · Cited by 6
“A few studies have shown the adsorption of nanoparticles to the exoskeleton of aquatic invertebrates (Dabrunz et al., 2011; Asghari et al., 2012); however, the mechanism of interaction between the nanoparticles and the cuticle is still not clear.”
Background
Effect of different surface functional groups of graphene on oxidative stress in Daphnia magna
Yao, H., Li, X., Zhang, L., Huang, Y. X. R., Luo, T., & Chen, J. (2018) · Chinese Science Bulletin (Chinese Version) · doi:10.1360/n972018-00960 · Cited by 6
Metal Nanoparticles in Surface Waters – a Risk to Aquatic Organisms
Tomczyk-Wydrych, I. (2019) · Bezpieczeństwo i Technika Pożarnicza · doi:10.12845/sft.51.3.2019.5 · Cited by 6
Toxicological Effects of Nanobiofertilizer on Water Body, Water Quality, Lower Plants, Zooplanktons, and Beneficial Microorganisms
Utazi, E. B., Oyewole, O. A., Yakubu, J. G., Yetu, T. P., Omoregie, I. P., Adetunji, C. O., Mathew, J. T., Igiku, V., Eniola, K. I. T., & Yerima, M. B. (2024) · doi:10.1002/9781394211548.ch8 · Cited by 6
Toxicity and bioaccumulation of nanoparticles of zinc oxide (ZnO) and titanium dioxide (TiO2) in Chydorus sphaericus and Cypridopsis cf. vidua (Crustacea)
Hernández-Pedraza, M., Alvarado-Flores, J., Silva-Briano, M., Adabache-Ortíz, A., & Rico‐Martínez, R. (2025) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2025.104661 · Cited by 5
Effects of TiO2 Nanoparticles on the Neotropical Cladoceran Ceriodaphnia silvestrii by Waterborne and Dietary Routes
de Lucca, G. M., Freitas, E. C., & Melão, M. D. G. G. (2018) · Water Air & Soil Pollution · doi:10.1007/s11270-018-3964-1 · Cited by 5
“In the literature, not surprisingly, the use of nontarget species results in a wide variety of responses (EC50) in acute toxicity tests with TiO2 NPs (Amiano et al. 2012; Clément et al. 2013; Dabrunz et al. 2011; Griffitt et al. 2008; Zhu et al. 2010a, b).”
Background
Nematode surface functionalization with hydrogel sheaths tailored in situ
Mubarok, W., Nakahata, M., Kojima, M., & Sakai, S. (2022) · Materials Today Bio · doi:10.1016/j.mtbio.2022.100328 · Cited by 5
“Recent advances in encapsulation technology have allowed the modification of cell surfaces with various materials, for instance, mammalian cells with hydrogels [1], yeast with iron nano-shells [2], and Chlorella and Daphnia magna with titanium oxide shells [3,4].”
Background
Nano-immobilized flumequine with preserved antibacterial efficacy
Bortoletti, M., Molinari, S., Fasolato, L., Ugolotti, J., Tolosi, R., Venerando, A., Radaelli, G., Bertotto, D., Liguoro, M. D., Salviulo, G., et al. (2020) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2020.111019 · Cited by 5
Subchronic Effects of Ectoine on Survival, Growth and Physiological Parameters of Daphnia Magna
Zofia, B. A. S. (2015) · Journal of Aquaculture Research & Development · doi:10.4172/2155-9546.1000352 · Cited by 5
“Moulting A lack of food and toxic effects induced by some chemicals may inhibit growth of neonates and thereby decrease moulting frequency [39-42].”
Background
Erratum to: Polyvinylpyrrolidone and arsenic-induced changes in biological responses of model aquatic organisms exposed to iron-based nanoparticles
Llaneza, V., Rodea‐Palomares, I., Zhou, Z., Rosal, R., Fernández‐Piñas, F., & Bonzongo, J. J. (2016) · Journal of Nanoparticle Research · doi:10.1007/s11051-016-3604-x · Cited by 5
Fate and biological effects of titanium dioxide nanoparticles in the aquatic environment
Li, L. (2017) · Työväentutkimus Vuosikirja · Cited by 5
Ecological fitness impairments induced by chronic exposure to polyvinyl chloride nanospheres in Daphnia magna
Masseroni, A., Federico, L., & Villa, S. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e40065 · Cited by 4
“This can lead to alterations in the molting behaviour as a possible pathway for physical nanoparticle toxicity [59,60].”
Nanosized titanium dioxide elevates toxicity of cationic metals species for Daphnia – have aging and natural organic matter an unexpected impact?
Roy, R., Kandrapu, V. K., Kempter, L., Islam, R., Kalčíková, G., Schulz, R., & Bundschuh, M. (2022) · Nanotoxicology · doi:10.1080/17435390.2022.2027538 · Cited by 4
Toxicity Tests and Bioassays for Aquatic Ecotoxicology of Engineered Nanomaterials
Schmidt, S. I., Kühnel, D., & Kokalj, A. J. (2019) · CRC Press eBooks · doi:10.1201/9781315158761-4 · Cited by 4
Nanotechnology From Engineers to Toxicologists
Anwar, W., & Khitab, A. (2019) · International Journal of Applied Nanotechnology Research · doi:10.4018/ijanr.2019070101 · Cited by 4
Nanomaterialien: Auswirkungen auf Umwelt und Gesundheit
TA-SWISS (2013) · vdf Hochschulverlag AG an der ETH Zürich eBooks · doi:10.3218/3560-5 · Cited by 4
Effects of copper in Daphnia are modulated by nanosized titanium dioxide and natural organic matter: what is the impact of aging duration?
Roy, R., Lüderwald, S., Maknoon, A. A. A., Metreveli, G., Schulz, R., & Bundschuh, M. (2020) · Environmental Science and Pollution Research · doi:10.1007/s11356-020-11578-2 · Cited by 4
“All comparisons discussed in this paper are based on 48 h Cu EC50 values, as effects caused by Cu after 24 h, 72 h and 96 h of exposure were either low (24 h) or already disguised by nTiO2 toxicity (72 h and 96 h) (Dabrunz et al. 2011).”
Method
Adsorption of potentially toxic metals on negatively charged liposomes: equilibrium isotherms and quantitative modeling
Yu, Y., Liu, X., Gong, W., Liu, G., Cheng, D., Huaying, B., & Gao, D. (2014) · RSC Advances · doi:10.1039/c4ra04775c · Cited by 4
Getting over it? A proteomic analysis of mechanisms driving multigenerational acclimation to organic ultraviolet filters in Daphnia magna
Boyd, A., Lummer, C., Mehta, D., Uhrig, R. G., & Blewett, T. A. (2025) · Environmental Pollution · doi:10.1016/j.envpol.2025.126934 · Cited by 3
Practical considerations to optimize aquatic testing of particulate material, with focus on nanomaterials
Lüderwald, S., Davies, J., Fernandes, T. F., Praetorius, A., Sergent, J., Tatsi, K., Tell, J. G., Timmer, N., & Wagner, S. (2024) · Environmental Science Nano · doi:10.1039/d4en00056k · Cited by 3
“42 and 43)).”
Background
Modifying the aquatic toxicity of Co3O4 nanoparticles in exposed microalgae by CTAB mediated synthesis
Sharan, A., & Nara, S. (2024) · Biocatalysis and Agricultural Biotechnology · doi:10.1016/j.bcab.2024.103111 · Cited by 3
Umweltauswirkungen künstlich hergestellter Nanomaterialien
Greßler, S., & Nentwich, M. (2014) · Springer eBooks · doi:10.1007/978-3-7091-1405-6_2 · Cited by 3
Toxicity of Titanium Dioxide Nanoparticles on Brain
Shao, L., & Song, B. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-804598-5.00005-2 · Cited by 3
A review of the toxicity of nanoparticles to Daphnia magna
Yi, H. U., Wang, Y., & Lin, D. (2017) · Chinese Science Bulletin (Chinese Version) · doi:10.1360/n972017-00476 · Cited by 3
Distribution and trophic transfer of engineered nanoparticles along aquatic food chains and related influencing factors: A review
Zhao, J. L., Xu, L., Yin, S., Li, Y., Wang, Z., Hou, R., Yao, H., Dai, Y., & Liu, Z. (2018) · Chinese Science Bulletin (Chinese Version) · doi:10.1360/n972018-00021 · Cited by 3
Toxicological Effects of Nanobiofertilizer on Water Body, Water Quality, Lower Plants, Zooplanktons, and Beneficial Microorganisms
Utazi, E. B., Oyewole, O. A., Yakubu, J. G., Yetu, T. P., Omoregie, I. P., Adetunji, C. O., Mathew, J. T., Igiku, V., Eniola, K. I. T., & Yerima, M. B. (2024) · doi:10.1002/9781394234769.ch63 · Cited by 3
Cytotoxicity and Genotoxicity Effects of a Magnetic Zeolite Composite in Daphnia magna (Straus, 1820)
Zarria-Romero, J. Y., & Ramos‐Guivar, J. A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25147542 · Cited by 2
“Another study found that exposure to TiO 2 NPs caused the interruption of molting [52].”
Background
Nanotoxicity: A Mechanistic Approach
Gupta, I. R., Gaikwad, S. C., Ingle, A. P., Kon, K. V., Durán, N., & Rai, M. (2015) · CRC Press eBooks · doi:10.1201/b18654-20 · Cited by 2
NANOBIOTECHNOLOGY AS A PROSPECTIVE APPROACH FOR SAFE ENVIRONMENTAL REMEDIATION - A REVIEW
Kumari, A., & Sobha, K. (2013) · International Journal of Pharma and Bio Sciences · Cited by 2
Nano and Environment - Part II: Hazard potentials and risks (NanoTrust Dossier No. 027en - March 2012)
Greßler, S., & Nentwich, M. (2012) · doi:10.1553/ita-nt-027en · Cited by 2
Retraction: Case study: three dimensional analysis of the swimming behaviour of daphnia magna exposed to nanosized titanium dioxide
Charde, M. S., Ingole, P. V., Welankiwar, A. S., Kumar, J., & Chakole, R. D. (2014) · International Journal of Pharmacological Research · doi:10.7439/ijpr.v4i2.95 · Cited by 2
Toxicity of Engineered Nanoparticles to Aquatic Invertebrates
Cupi, D., Sørensen, S. N., Skjolding, L. M., & Baun, A. (2016) · doi:10.1002/9781119275855.ch19 · Cited by 2
Fitness related effects of titanium dioxide nanoparticles and glyphosate exposure on Cardiocondyla obscurior
Nyckees, D., de Vega, R. G., Sittinger, R., Clases, D., & Freitak, D. (2026) · Environmental science and pollution research international · doi:10.1007/s11356-025-37388-y · Cited by 1
“There have been few studies that investigated the toxicological effect of TiO 2 NPs, providing evidence of detrimental consequences on terrestrial and aquatic animals (Federici et al. 2007; Dabrunz et al. 2011; Libralato et al. 2013; Wang et al. 2013, 2019).”
Combined effect of polyethylene microplastics and Microcystis aeruginosa spent medium on Daphnia magna
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Authors: Dabrunz, A., Duester, L., Prasse, C., Seitz, F., Rosenfeldt, R., Schilde, C., Schaumann, G. E., & Schulz, R.
Affiliations: University of Koblenz and Landau (DE)
Technische Universität Braunschweig (DE)
Corresponding author: Schulz, Ralf
ORCID: Duester, Lars
Prasse, Carsten
Seitz, Frank
Schilde, Carsten
Schaumann, Gabriele E.
Schulz, Ralf
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2011-05-27
Volume: 6
Issue: 5
Pages: e20112
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0020112
PMC: PMC3103543
OpenAlex: W1971246481
Cited by: 208
References: 38
Citations by year: 2026: 4 · 2025: 4 · 2024: 7 · 2023: 9 · 2022: 12 · 2021: 10 · 2020: 14 · 2019: 15 · 2018: 17 · 2017: 13 · 2016: 26 · 2015: 22 · 2014: 22 · 2013: 13 · 2012: 14
FWCI: 12.45
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics: Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
Physical Sciences › Materials Science › Materials Chemistry › Nanoparticles: synthesis and applications
Physical Sciences › Environmental Science › Pollution › Microplastics and Plastic Pollution
Keywords: titanium dioxide nanoparticles, nanoparticle toxicity, Daphnia magna, molting inhibition, particle size effects, freshwater zooplankton, ecotoxicology, long-term exposure
MeSH terms: Animals, Daphnia, Dose-Response Relationship, Drug, Particle Size, Suspensions, Time Factors, Titanium, Water, Molting, Nanoparticles

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Biological Surface Coating and Molting Inhibition as Mechanisms of TiO2 Nanoparticle Toxicity in Daphnia magna

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