ARTICLE pubs.acs.org/est
TiO2 Nanoparticles in the Marine Environment: Impact on the Toxicity of Tributyltin to Abalone (Haliotis diversicolor supertexta) Embryos Xiaoshan Zhu,† Jin Zhou,† and Zhonghua Cai* Marine Biology Laboratory of Life Sciences Division, Graduate School at Shenzhen, Tsinghua University, Shenzhen 518055, China
bS Supporting Information ABSTRACT: Little information is available on the potential ecotoxicity of manufactured nanomaterials (MNMs) in the marine environment. To carefully address this issue, the toxicity of nanosized titanium dioxide (nTiO2) aggregates in the marine environment was evaluated using abalone (Haliotis diversicolor supertexta) embryonic development as a model. The effect of nTiO2 aggregates on the toxicity of the highly toxic marine antifouling compound tributyltin (TBT) to abalone embryos was also investigated. No developmental effects of nTiO2 were observed at 2 mg/L but concentrations g10 mg/L caused hatching inhibition and malformations. The presence of 2 mg/L nTiO2 increased the toxicity of TBT up to 20-fold compared with TBT alone. This enhancement of TBT may be due to the combined effects of TBT adsorption onto nTiO2 aggregates and the internalization of nTiO2 aggregates by abalone embryos. These observations indicate that MNMs may have important indirect impacts on aquatic organisms by varying the toxicity of coexisting pollutants. Thus, risk assessments for MNMs should consider both their direct effects and possible indirect effects of interactions with other environmental contaminants.
’ INTRODUCTION Nanosized titanium dioxide (nTiO2) is one of the most popular manufactured nanomaterials (MNMs) increasingly being incorporated into a variety of consumer products. TiO2 nanoparticles are added to sunscreens, cosmetics, paints, and surface coatings,1,2 and are used in the decontamination of air, soil, and water.3,4 These wide applications have led to a rapid increase in the production of nTiO2, which, in the United States, is estimated to reach 2.5 106 tons per year by 2025.5 Environmental contamination by nTiO2 from urban applications seems inevitable and raises concerns with respect to the exposure of aquatic organisms to nTiO2.6,7 Industrial and urban effluents are often discharged into estuarine or marine environments, while Kaegi et al.6 reported that nTiO2 released from painted facades has concentrations as high as 3.5 108 particles/L in the runoff water. Keller et al.8 conducted a detailed analysis of the properties and behavior of MNMs, including nTiO2, in a range of natural waters. The high ionic strength (IS) and low organic carbon concentration of seawater causes MNMs to aggregate into much larger particles,8,9 which tend to settle out of solution. Consequently, sediments and benthic organisms are expected to be the main sink, and the ultimate receptor, for MNMs in the marine environment.10,11 Risk assessments of the release of these compounds must therefore take account of their effects on marine benthic organisms. TiO2 nanoparticles are toxic to bacteria, cell lines, and rodents, but little is known about their toxicity to aquatic biota, especially to marine organisms.10,11 Miller et al.12 reported that nTiO2 had no measurable effect on the growth of marine phytoplankton. r 2011 American Chemical Society
However, because of the sedimentation characteristics of MNMs, we predicted that benthic animals would be more susceptible to intoxication. To test this hypothesis in the present study, we examined the effects of nTiO2 on the development of the marine benthic embryos of the abalone (Haliotis diversicolor supertexta). The abalone is an appropriate model organism because it is a common benthic gastropod inhabiting the coastal environment, and is a sensitive indicator of coastal pollution.13 The abalone embryo test has been proposed as a standard method to evaluate the toxicological effects of environmental pollutants in coastal areas.14 Because of their high surface area, MNMs are able to adsorb a variety of contaminants from aquatic environments, forming nanoparticletoxin complexes.10,11 Binding of trace metals to colloids and their subsequent concentration and transfer from the water column to sediments by aggregation and settling is termed colloidal pumping.10,11,15 It is speculated that an analogous binding of other marine pollutants to MNMs to form nanoparticletoxin complexes could also result in the accumulation of pollutants in the sediments.10,16 Thus, we hypothesized that the presence of nTiO2 might exacerbate the toxicity of other pollutants. To test this hypothesis, we compared the effects of nTiO2 aggregates and tributyltin (TBT), alone and in combination, on abalone embryonic development, and on the uptake of Received: November 9, 2010 Accepted: March 8, 2011 Revised: February 28, 2011 Published: March 17, 2011 3753
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TBT by the embryos. TBT is a highly toxic antifouling compound used in many industrial processes and has been widely introduced into marine environments in antifouling paints.17 Its toxicity to humans and aquatic animals has been intensely studied (reviewed in ref 18). Among its effects is the induction of imposex and reproductive failure in marine mollusks.19 TBT has also been reported to induce oxidative damage in animals, including abalone.20,21 Therefore, analyses of oxidative stress indicators were performed at the end of the embryo toxicity tests to better understand the influence of nTiO2 on the toxicity induced by TBT.
’ MATERIALS AND METHODS nTiO2 Solutions. Uncoated nTiO2 with a published particle size e10 nm was purchased from Nanjing High Technology Nano Material Co., Ltd. (Nanjing, China). It was supplied as a white anatase powder, with a purity g99.5% and a specific surface area g150 m2/g. A stock solution of 10 g/L nTiO2 was prepared by dispersing the nanoparticles in ultrapure water (Millipore, Billerica, MA, USA) with sonication for 10 min (50 W/L, 40 kHz). Test solutions of nTiO2 were prepared immediately prior to use by diluting the stock solution with fresh sand-filtered seawater (SFS, 24 ( 2 °C, salinity 30 ( 2%, pH 8.0 ( 0.2, dissolved oxygen g7.0 mg/L, TBT undetectable). Further information on particle size distribution and morphology, and sedimentation characteristics of the test solution is provided in the Supporting Information. TBT Solutions. Stock solutions of TBT chloride (purity >99%; Wako Pure Chemicals, Osaka, Japan) were prepared in acetone (99.5%, reagent grade). A series of test solutions (0.4, 2, 10, and 50 ng/L), based on environmentally realistic levels of TBT,22 were obtained by dilution of the corresponding stocks with SFS. Adsorption of TBT onto nTiO2. To examine the formation of nTiO2TBT complexes in the marine environment, the adsorption of TBT onto nTiO2 nanoparticles in SFS was examined. The adsorption isotherm was determined by varying the initial TBT concentration (2, 10, 50, 100, 500, and 1000 ng/L) at a fixed TiO2 concentration (2 mg/L). After 9 h (the duration of toxicity tests), the residual TBT concentration in the aqueous phase (Cw, ng/L) was measured by gas chromatography with flame photometric detection (GC-FPD, Thermo Scientific, FL, USA),23 and calibrated using the TBT control solutions without nTiO2. The detection limit of this method was 1.0 ng/L. The adsorbed TBT concentration (Cs, ng/mg nTiO2) was calculated assuming mass balance between the initial and the final solutions. The Freundlich sorption isotherm (log Cs = n log Cw þ log KF, where n and KF are the Freundlich coefficients) was determined by linear regression.24,25 Toxicity of nTiO2. Mature abalones were collected from a local hatchery (Shenzhen, China). Details of the culture and spawning processes are presented in the Supporting Information. Fertilized eggs (embryos) were used for all experiments. Embryos (∼5 104 per test) were cultured in 500 mL of SFS in porcelain beakers containing a range of nTiO2 concentrations (2, 10, 50, and 250 mg/L). SFS without added nTiO2 was included as the control. The appearance of the first polar body at 0.25 h post fertilization (hpf) indicated fertilization success. Development was observed using an inverted microscope (AE30, Motic, Xiamen, China) at specific times. The multicell stage (0.52 hpf) was examined to assess cleavage inhibition. Embryo malformations
Figure 1. Hatching rate (upper) and malformation rate (lower) of abalone embryos exposed to different concentrations and combinations of TBT and nTiO2. The controls were sand-filtered seawater (SFS) and SFS containing acetone at the highest concentrations used in the TBT treatments. Significance differences (p < 0.05) are indicated: * vs seawater control; # vs 2 mg/L nTiO2 treatment; and a,b,c,d nTiO2þTBT treatments vs the corresponding TBT only treatment.
were identified between the blastula stage (34 hpf) and the trochophore larva, just prior to hatching (89 hpf). Embryos with developmental delay, epidermal edema, yolk leakage, protuberances on body surfaces, or other morphological defects were all considered malformed. Each treatment was repeated at least 5 times. The malformation rate (%) was calculated from the number of malformed embryos among the total number of embryos observed. To determine hatching rates, 200 embryos were removed from each test beaker at 8 hpf (just before the trochophores were ready to hatch), transferred to a 50-mL glass beaker, and observed until 1213 hpf. The embryos which failed to hatch were counted and the hatching rate (%) was calculated by difference. Toxicity of TBT With and Without nTiO2. The toxicity of TBT, in the absence or presence of nTiO2 (2 mg/L), was determined by a test procedure similar to that described above for nTiO2. For tests without nTiO2, selected embryos were exposed to 4 concentrations (0.4, 2, 10, and 50 ng/L) of TBT. For tests including nTiO2, TBT test solutions were prepared and mixed with 2 mg/L nTiO2 prior to exposure. Appropriate SFS control groups, containing either nTiO2 alone, or acetone at the highest concentration present in the TBT treatments, were included in each test run. After calculation of the malformation and hatching rates, the embryos from each treatment were collected at 89 hpf, rinsed with fresh SFS, and stored at 20 °C for biochemical analysis. Biochemical parameters for oxidative stress, including the activity of superoxide dismutase (SOD), reduced glutathione (GSH) content, and lipid peroxidation (LPO) levels, were determined using a Diagnostic Reagent Kit (Nanjing Jiancheng 3754
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Figure 2. Examples of malformations (indicated by arrows) in abalone embryos exposed to TBT and nTiO2 alone or in combination. The control was sand-filtered seawater containing acetone at the highest concentrations used in the TBT treatments. Times indicated are hours post fertilization (hpf): 0.52 hpf: multicell stage; 34 hpf: blastula stage; and 68 hpf: complete formation of the prototrochal girdle. C: cloudy appearance indicating dead embryos; D: developmental delay; E: epidermal edema; P: protuberances on the body surface; Y: yolk leakage. (10 10).
Bioengineering Institute, Nanjing, China). Details of the procedures are provided in the Supporting Information. Uptake of TBT in Embryos in the Presence and Absence of nTiO2. Embryos were exposed to 50 ng/L TBT with and without nTiO2 (2 mg/L) and analyzed to determine their TBT content. Samples of 13 g (wet weight) were taken at 8 hpf, rinsed twice with ultrapure water for 15 s to remove external nTiO2 adsorbed to the chorion of the embryos, and analyzed for TBT by GC-FPD.23 Whole body burden of TBT was expressed as ng/g wet weight. TEM Analysis of the Internalization of nTiO2. Embryos were taken from the SFS control, the 2 mg/L nTiO2, and the 2 mg/L nTiO2 þ 50 ng/L TBT treatments at 8 hpf, and fixed with 2.5% glutaraldehyde in 0.1 M phosphate buffer. They were then washed in 0.1 M cacodylate buffer, postfixed with 1% osmium tetroxide, washed again in buffer, dehydrated, and embedded in Epon 812. Ultrathin sections (7090 nm thick) prepared using an ultramicrotome (Leica EM UC6, Germany) were mounted on 150-mesh copper grids and examined by transmission electron microscopy (TEM) at 80 kV (Hitachi H-7650). The presence of nTiO2 inside the embryos was confirmed by energy dispersive X-ray analysis (EDS). Data Analyses. All the tests in this study were conducted in triplicate. Values are expressed as means ( standard deviation (SD). The EC50 and the associated 95% confidence intervals (95% CI) were calculated by Probit Analysis (USEPA software, version 1.5). The no observed effect concentration (NOEC) was defined as the highest tested concentration which, when compared with the control, had no statistically significant effect within the exposure period.26 One-way analysis of variance (ANOVA) with Tukey’s multiple comparisons was used to compare the differences between groups. Differences were considered statistically significant when p < 0.05.
’ RESULTS AND DISCUSSION Characterization and Sedimentation of nTiO2 in Seawater. In SFS, nTiO2 formed large aggregates ranging in
diameter from 562 nm to 22.7 μm, as detected by dynamic light scattering (DLS), although smaller (e500 nm) aggregates were
observed using TEM (see Supporting Information Figure S1). After 9 h, 61% of the nTiO2 had left the water column and settled on the bottom of the beaker (Figure S2). A layer of these settled aggregates could be observed with the naked eye, particularly at the higher concentrations tested. These observations are consistent with those of Keller et al.8 that the high IS of seawater facilitates the aggregation of nanoparticles. Direct Toxicity of nTiO2 on Embryonic Abalone. No significant inhibition of hatching or malformations were observed in the 2 mg/L nTiO2 treatment groups (Figure 1). However, the hatching rate was significantly lower than that of the control at exposure concentrations g10 mg/L, consistent with a dose-dependent inhibition. Significant malformations, including developmental delay and protuberances on the body surfaces, occurred in the 10 mg/L treatment group, affecting 29.5% of abalone embryos (Figures 1 and 2). At higher nTiO2 concentrations, the rate and severity of malformations increased. The NOECs of nTiO2 for hatching inhibition and malformation of abalone embryos were approximately 2 mg/L and the EC50 values were 56.9 mg/L and 345.8 mg/L, respectively (Table 1). The mechanisms responsible for the toxicity of nTiO2 in marine environments are unknown. In the present study, direct adherence/adsorption of nTiO2 aggregates to the outer envelope (chorion) of abalone embryos was observed (Figure S3). Previous studies have demonstrated the adherence of nTiO2, singlewall carbon nanotubes (SWCNT), and C60 agglomerates to the outer layer of zebrafish embryos and to algal cells.6,24,27,28 Such attachment might cause physical changes in the surface mechanical properties of the organism, leading to the observed toxicity. For example, the hatching delay may be caused by a change in the elasticity of the chorion or by interference with the digestive function of the chorionic hatching enzyme.6,27 Alternatively, partial covering of the chorion of the nTiO2-exposed embryos might interfere with oxygen uptake, resulting in internal hypoxia. Delayed development and hatching of embryos has been attributed to hypoxia in previous studies.27 Contact with nZnO has been reported to disrupt membrane structure in Escherichia coli cells, leading to an increase in membrane permeability, accumulation 3755
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Table 1. EC50 Values for the Different Treatments hatching inhibition treatments
malformation
EC50 values (10 h)
95% CI
EC50 values (8 h)
95% CI
nTiO2
56.9 mg/L
28.0126.3
345.8 mg/L
155.01592.6
TBT
46.5 ng/L
41.551.3
13.4 ng/L
9.717.2
nTiO2 þ TBT
2.1 ng/L
1.52.8
1.9 ng/L
1.22.7
Enhanced Toxicity of TBT to Abalone Embryos in the Presence of nTiO2. The Freundlich sorption isotherm equation
Figure 3. TEM images of ultrathin sections of the embryos exposed to (A) seawater control; (B) 2 mg/L nTiO2; (C, E) nTiO2 þ 50 ng/L TBT. (D) and (F) are enlarged from (C) and (E), respectively. No nTiO2 was present in the control and 2 mg/L nTiO2-treated embryos (A, B). However, internalized nTiO2 was present near the chorion (D) and in the cytoplasm (E) of TiO2 þ TBT-exposed embryos. (G) EDS of TiO2 þ TBT-exposed embryos, confirming the presence of nTiO2.
of nZnO in the membrane, and internalization of these nanoparticles (NPs).29 In contrast, TEM observation of abalone embryos indicated no internalization of nTiO2 in the embryos exposed to nTiO2 alone (Figure 3). This suggests that the membrane permeability of abalone embryos was not affected by nTiO2, which is consistent with observations on SWCNT in zebrafish embryos.24,27,28 Another possibility is that observed developmental toxicity associated with the adherent nTiO2 aggregates might have been caused by excessive production of reactive oxygen species (ROS).30 Previous studies have suggested that oxidative stress could contribute to nTiO2-mediated toxicity in freshwater fish.31,32 More research is needed to evaluate the relative importance of physical effects versus oxidative stress in nTiO2-mediated toxicity.
for binding of TBT to 2 mg/L nTiO2 was log Cs = 1.59 log Cw 1.98 (R2 = 0.92). The adsorption of TBT onto nTiO2 was fast, reaching a steady state within 120240 min. After 9 h, the residual TBT remaining in a test solution, which initially contained 100 ng/L TBT and 2 mg/L nTiO2, stabilized at 28.6% of the initial concentration, the balance presumably being bound to nTiO2 particles (Figures S4 and S5). To assess the impact of the formation of nTiO2TBT complexes on the toxicity of TBT, we observed the development of abalone embryos in SFS containing a range of TBT concentrations, in the presence and absence of nTiO2 aggregates. When TBT alone was added, the lowest concentrations (0.4 and 2 ng/ L) produced no significant change in either malformation or hatching rates compared with controls (Figure 1). However, in the presence of 2 mg/L nTiO2, a significant decrease in hatching rate and an increase in malformation rate was observed relative to controls at all TBT concentrations, and (except for the hatching rate in 50 ng/L TBT) was also relative to the corresponding TBT treatment without nTiO2 (Figure 1). Thus, the EC50 of TBT for embryo hatching and malformations decreased from 46.5 and 13.4 ng/L without addition of nTiO2 to 2.11 and 1.87 ng/L, respectively, after adding nTiO2 (Table 1), i.e., 20-fold and 7-fold greater toxicity for embryo hatching and malformations, respectively. Although the rate of malformation increased with the addition of nTiO2, the types of malformation (cloudy appearance, developmental delay, epidermal edema, protuberances on the body surfaces, yolk leakage) were similar between the groups with and without nTiO2 (Figure 2). Indicators of oxidative damage caused by TBT, with and without added nTiO2, are compared in Figure 4. SOD activities were significantly increased relative to controls in the groups treated with 0.4, 2, and 10 ng/L TBT alone, but not at 50 ng/L TBT. The addition of nTiO2 decreased SOD activity toward the control value, particularly at the two lowest TBT concentrations. GSH content was lower than the control values at the two highest TBT concentrations (10 and 50 ng/L) and was further lowered in the nTiO2 þ TBT treatment groups. LPO levels were significantly elevated relative to controls in the 2, 10, and 50 ng/L TBT groups and were further increased following the addition of nTiO2. Taken together, these measurements are consistent with earlier reports that TBT induces oxidative stress in organisms.20,21 This suggests that nTiO2 exacerbates the stress and the toxicity of TBT in the marine environment. Possible Mechanisms for the Enhanced Toxicity of TBT in the Presence of nTiO2. We showed that TBT was absorbed onto nTiO2 aggregates to form nTiO2TBT complexes (Figures S4 and S5). Therefore, the aggregation and subsequent sedimentation of nTiO2 led to the accumulation of TBT at the bottom of the experimental beaker, which likely increased the exposure risk for demersal embryos. It is also possible that 3756
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Figure 4. Effects of TBT (0.450 ng/L) with and without nTiO2 (2 mg/L) on superoxide dismutase (SOD) activities, reduced glutathione (GSH) contents, and lipid peroxidation (LPO) levels in abalone embryos at 8 hpf. Significance differences (p < 0.05) are indicated by: * vs acetone control; a,b,c,d vs the corresponding TBT groups without nTiO2.
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might first damage the embryo surface and facilitate the internalization of nTiO2TBT complexes. To assess whether internalization of nTiO2 aggregates occurred, embryos treated with nTiO2 only, and with mixtures of TBT and nTiO2, were analyzed using TEM (Figure 4). No nTiO2 was taken up by embryos exposed only to nTiO2. However, internalized nTiO2 was observed in the embryos exposed to mixtures of TBT and nTiO2 (Figure 4). Because TBT was sorbed onto nTiO2, internalization of nTiO2 aggregates could accelerate the uptake of TBT, resulting in a cumulative toxic effect. The higher body burden of TBT in the embryos exposed to mixtures of TBT and nTiO2 (Figure 5) supports this interpretation. Previous studies have suggested that direct contact with NPs may enhance the toxicity of pollutants to algae.24,25 Collectively, these results indicate that the indirect impact of NPs through their interactions with other environmental contaminants in ecosystems should not be neglected. In conclusion, we have demonstrated both direct and indirect toxicities of nTiO2 aggregates on a marine organism. The high IS in the marine environment facilitates the formation of large agglomerates of nTiO2, which tend to settle out of solution quickly. These nTiO2 aggregates are directly toxic to abalone embryos at high concentrations (g10 mg/L), delaying development, inhibiting hatching, and inducing malformations. We also report, for the first time, that the toxicity of TBT to abalone embryos is enhanced in the presence of nTiO2 aggregates, illustrating an important indirect impact of NPs on aquatic organisms. The toxicity enhancement of TBT may be due to the combined effect of TBT adsorption onto nTiO2 aggregates and the direct adherence/adsorption of nTiO2 onto the surface of abalone embryos. We conclude that risk assessments for NPs should focus not only on the direct impacts of their inherent properties but also should consider their interactions with other environmental pollutants.
’ ASSOCIATED CONTENT
bS
Supporting Information. Procedures for abalone culture and spawning, and for biochemical analysis of oxidative stress parameters; TEM images and size distribution of nTiO2 aggregates in seawater; sedimentation rate of nTiO2 aggregates in seawater; adherence of nTiO2 aggregates to embryos; adsorption kinetics and Freundlich plot of adsorption of TBT onto TiO2 aggregates. This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author Figure 5. Uptake of TBT with and without nTiO2 in abalone embryos at 8 hpf. Different letters indicate significant differences (p < 0.05) between treatments. nd, not detected.
adherence of nTiO2 aggregates to the surface of abalone embryos contributed to the enhanced toxicity. This adherence of the nTiO2 aggregates (sorbed with TBT) to the surface of abalone embryos potentially delivered TBT directly to the embryos. As the toxicity of TBT increased significantly in the presence of nTiO2, it seems that at least some of the complexed TBT must be available to the abalone embryos. Furthermore, as 2 mg/L nTiO2 caused no observable effects in the embryos (Figure 1), TBT
*Address: Marine Biology Laboratory of Life Sciences Division, Graduate School at Shenzhen, Tsinghua University, Rm 304, Bd L, Tsinghua Campus, University Town, Shenzhen 518055, China; phone: þ86-755-26036108; fax: þ86-755-26036108; e-mail:
[email protected]. Author Contributions †
These authors contributed equally to this work.
’ ACKNOWLEDGMENT This project was supported in part by the special fund of State Key Joint Laboratory of Environment Simulation and Pollution Control (10K10ESPCT), and by the Key Laboratory of Marine 3757
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Environmental Science & Technology Ecology and Environmental Science and Engineering, SOA (MESE-2010-02). We thank Dr. Xingliang Jin (Director of the Animal and Plant Inspection and Quarantine Center of Shenzhen Guangmin District) and Xingxing Jin for their help in measuring TBT. We also thank the anonymous reviewers for their valuable comments on this manuscript.
’ REFERENCES (1) Kaida, T.; Kobayashi, K.; Adachi, M.; Suzuki, F. Optical characteristics of titanium oxide interference film and the film laminated with oxides and their applications for cosmetics. J. Cosmet. Sci. 2004, 55 (2), 219–20. (2) Fisher, J.; Egerton, T. Kirk-Othmer Encyclopedia of Chemical Technology; John Wiley: New York, 2001. (3) Choi, H.; Stathatos, E.; Dionysiou, D. D. Sol-gel preparation of mesoporous photocatalytic TiO2 films and TiO2/Al2O3 composite membranes for environmental applications. Appl. Catal., B 2006, 63 (12), 60–67. (4) Esterkin, C. R.; Negro, A. C.; Alfano, O. M.; Cassano, A. E. Air pollution remediation in a fixed bed photocatalytic reactor coated with TiO2. AIChE J. 2005, 51 (8), 2298–2310. (5) Robichaud, C. O.; Uyar, A. E.; Darby, M. R.; Zucker, L. G.; Wiesner, M. R. Estimates of Upper Bounds and Trends in Nano-TiO2 Production As a Basis for Exposure Assessment. Environ. Sci. Technol. 2009, 43 (12), 4227–4233. (6) Kaegi, R.; Ulrich, A.; Sinnet, B.; Vonbank, R.; Wichser, A.; Zuleeg, S.; Simmler, H.; Brunner, S.; Vonmont, H.; Burkhardt, M.; Boller, M. Synthetic TiO2 nanoparticle emission from exterior facades into the aquatic environment. Environ. Pollut. 2008, 156 (2), 233–9. (7) Kiser, M. A.; Westerhoff, P.; Benn, T.; Wang, Y.; Perez-Rivera, J.; Hristovski, K. Titanium nanomaterial removal and release from wastewater treatment plants. Environ. Sci. Technol. 2009, 43 (17), 6757–63. (8) Keller, A. A.; Wang, H.; Zhou, D.; Lenihan, H. S.; Cherr, G.; Cardinale, B. J.; Miller, R.; Ji, Z. Stability and aggregation of metal oxide nanoparticles in natural aqueous matrices. Environ. Sci. Technol. 2010, 44 (6), 1962–7. (9) Zhu, X.; Wang, J.; Zhang, X.; Chang, Y.; Chen, Y. The impact of ZnO nanoparticle aggregates on the embryonic development of zebrafish (Danio rerio). Nanotechnology 2009, 20 (19), 195103. (10) Klaine, S. J.; Alvarez, P. J.; Batley, G. E.; Fernandes, T. F.; Handy, R. D.; Lyon, D. Y.; Mahendra, S.; McLaughlin, M. J.; Lead, J. R. Nanomaterials in the environment: Behavior, fate, bioavailability, and effects. Environ. Toxicol. Chem. 2008, 27 (9), 1825–51. (11) Ward, J. E.; Kach, D. J. Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. Mar. Environ. Res. 2009, 68 (3), 137–42. (12) Miller, R. J.; Lenihan, H. S.; Muller, E. B.; Tseng, N.; Hanna, S. K.; Keller, A. A. Impacts of metal oxide nanoparticles on marine phytoplankton. Environ. Sci. Technol. 2010, 44 (19), 7329–34. (13) Gorski, J.; Nugegoda, D. Toxicity of trace metals to juvenile abalone, Haliotis rubra following short-term exposure. Bull. Environ. Contam. Toxicol. 2006, 77 (5), 732–40. (14) Liu, Y.; Guan, Y.; Yang, Z.; Cai, Z.; Mizuno, T.; Tsuno, H.; Zhu, W.; Zhang, X. Toxicity of seven phthalate esters to embryonic development of the abalone Haliotis diversicolor supertexta. Ecotoxicology 2009, 18 (3), 293–303. (15) Honeyman, B. D.; Santschi, P. H. The role of particles and colloids in the transport of radionuclides and trace metals in the ocean. In Environmental Particles; Buffle, J., Van Leeuwen, H. P., Eds.; Lewis Publishers Inc.: Boca Raton, FL, USA, 1992; Vol. 1, pp 379423. (16) Sigg, L. The regulation of trace elements in lakes: The role of sedimentation. In The Chemical and Biological Regulation of Aquatic Systems; Buffle, J., Devitre, R. R., Ed.; Lewis Publisher Inc.: Boca Raton, FL, USA, 1994; pp 175195.
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(17) Botton, M. L.; Hodge, M.; Gonzalez, T. I. High tolerance to tributyltin in embryos and larvae of the horseshoe crab, Limulus polyphemus. Estuaries 1998, 21 (2), 340–346. (18) Horiguchi, T.; Kojima, M.; Takiguchi, N.; Kaya, M.; Shiraishi, H.; Morita, M. Continuing observation of disturbed reproductive cycle and ovarian spermatogenesis in the giant abalone, Haliotis madaka from an organotin-contaminated site of Japan. Mar. Pollut. Bull. 2005, 51 (812), 817–22. (19) Antizar-Ladislao, B. Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment. A review. Environ. Int. 2008, 34 (2), 292–308. (20) Jia, X. W.; Zhang, Z. P.; Wang, S. H.; Lin, P.; Zou, Z. H.; Huang, B. Q.; Wang, Y. L. Effects of tributyltin (TBT) on enzyme activity and oxidative stress in hepatopancreas and hemolymph of small abalone, Haliotis diversicolor supertexta. Chin. J. Oceanol. Limnol. 2009, 27 (4), 816–824. (21) Liu, H. G.; Wang, Y.; Lian, L. J.; Xu, L. H. Tributyltin induces DNA damage as well as oxidative damage in rats. Environ. Toxicol. 2006, 21 (2), 166–171. (22) Thomas, K. V.; Fileman, T. W.; Readman, J. W.; Waldock, M. J. Antifouling paint booster biocides in the UK coastal environment and potential risks of biological effects. Mar. Pollut. Bull. 2001, 42 (8), 677–88. (23) Takahashi, S.; Tanabe, S.; Takeuchi, I. I.; Miyazaki, N. Distribution and specific bioaccumulation of butyltin compounds in a marine ecosystem. Arch. Environ. Contam. Toxicol. 1999, 37 (1), 50–61. (24) Baun, A.; Sorensen, S. N.; Rasmussen, R. F.; Hartmann, N. B.; Koch, C. B. Toxicity and bioaccumulation of xenobiotic organic compounds in the presence of aqueous suspensions of aggregates of nano-C(60). Aquat. Toxicol. 2008, 86 (3), 379–87. (25) Hartmann, N. B.; Von der Kammer, F.; Hofmann, T.; Baalousha, M.; Ottofuelling, S.; Baun, A. Algal testing of titanium dioxide nanoparticles--testing considerations, inhibitory effects and modification of cadmium bioavailability. Toxicology 2010, 269 (23), 190–7. (26) Zhang, Y.; Chen, Y.; Westerhoff, P.; Hristovski, K.; Crittenden, J. C. Stability of commercial metal oxide nanoparticles in water. Water Res. 2008, 42 (89), 2204–12. (27) Cheng, J.; Flahaut, E.; Cheng, S. H. Effect of carbon nanotubes on developing zebrafish (Danio rerio) embryos. Environ. Toxicol. Chem. 2007, 26 (4), 708–16. (28) Zhu, X.; Zhu, L.; Duan, Z.; Qi, R.; Li, Y.; Lang, Y. Comparative toxicity of several metal oxide nanoparticle aqueous suspensions to Zebrafish (Danio rerio) early developmental stage. J. Environ. Sci. Health A 2008, 43 (3), 278–84. (29) Brayner, R.; Ferrari-Iliou, R.; Brivois, N.; Djediat, S.; Benedetti, M. F.; Fievet, F. Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Lett 2006, 6 (4), 866–70. (30) Hassoun, E.; Kariya, C.; Williams, F. E. Dichloroacetate-induced developmental toxicity and production of reactive oxygen species in zebrafish embryos. J. Biochem. Mol. Toxicol. 2005, 19 (1), 52–58. (31) Federici, G.; Shaw, B. J.; Handy, R. D. Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): Gill injury, oxidative stress, and other physiological effects. Aquat. Toxicol. 2007, 84 (4), 415–30. (32) Hao, L.; Wang, Z.; Xing, B. Effect of sub-acute exposure to TiO2 nanoparticles on oxidative stress and histopathological changes in Juvenile Carp (Cyprinus carpio). J. Environ. Sci. (China) 2009, 21 (10), 1459–66.
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