Elsevier

Chemosphere

Volume 78, Issue 3, January 2010, Pages 209-215
Chemosphere

Toxicity and bioaccumulation of TiO2 nanoparticle aggregates in Daphnia magna

https://doi.org/10.1016/j.chemosphere.2009.11.013Get rights and content

Abstract

Little is known about the potential ecotoxicity of engineered nanoparticles (NPs) to aquatic organisms. To carefully address this issue, we conducted a comprehensive toxicity assessment, including modified acute (72 h) and chronic (21 d) toxicity tests as well as nTiO2 accumulation analysis using Daphnia magna as a model organism. We found that nTiO2 exerted minimal toxicity to daphnia within the traditional 48 h exposure time, but caused high toxicity when the exposure time was extended to 72 h. This demonstrated that exposure duration may be a contributing factor in NP-mediated toxicity. Moreover, upon chronic exposure to nTiO2 for 21 d, daphnia displayed severe growth retardation and mortality, as well as reproductive defects. Interestingly, a significant amount of nTiO2 was found accumulated in daphnia. However, these daphnia displayed difficulty in eliminating nTiO2 from their body, presenting increased bioconcentration factor (BCF) values. This high level of bioaccumulation may interfere with food intake and ultimately affect growth and reproduction. In summary, long-term exposure of aquatic organisms to nTiO2 may alter the growing status of these organisms at both individual and population levels, posing risks to aquatic ecosystems.

Introduction

With the rapid development of nanotechnology, the potential health hazards and environmental impacts of manufactured nanoparticles (NPs) are of concern (Service, 2005, Nel et al., 2006). Some types of NPs, e.g., nanosized titanium dioxide (nTiO2), are used in a variety of consumer products such as sunscreens, cosmetics, paints, and surface coatings (Fisher and Egerton, 2001, Kaida et al., 2004) as well as in the environmental decontamination of air, soil, and water (Esterkin et al., 2005, Choi et al., 2006). Such widespread use raises concern that nTiO2 could pose a risk to both ecosystems and human beings.

Until recently, most of the studies on the potential toxicity of nTiO2 have focused on mammals (such as mice and rats) and/or on different types of cell lines. These studies have revealed that inhalation of nTiO2 causes pulmonary inflammation in rats and mice (Warheit et al., 2005, Warheit et al., 2006, Warheit et al., 2007). Hepatic injury and myocardial damage also occurred in adult mice after their exposure to different sizes (25 and 80 nm) of TiO2 particles for 2 weeks (Wang et al., 2007). In a cytotoxicity study, anatase (10 and 20 nm) TiO2 particles were found to induce oxidative DNA damage, lipid peroxidation, and micronuclei formation, as well as to increase hydrogen peroxide and nitric oxide production in a human bronchial epithelial cell line (Gurr et al., 2005). Additionally, exposure of syrian hamster embryo (SHE) cells to 1 μg cm−2 TiO2 (<20 nm) for 12–72 h caused a significant dose-dependent increase in the formation of micronuclei and apoptosis (Rahman et al., 2002).

In comparison, studies on the ecotoxicity of nTiO2 are limited to a few reports on acute experiments. The first results come from Hund-Rinke and Simon (2006), which found a dose-dependent toxicity of TiO2 to green algae (Desmodesmus subspicatus) (EC50 = 44 mg L−1), but no such effect in tests on Daphnia magna. A more recent study found that neither nTiO2 nor bulk TiO2, even at concentrations of 20 g L−1, were toxic to bacteria (Vibrio fischeri), or crustaceans (D. magna and Thamnocephalus platyurus) (Heinlaan et al., 2008). In addition, no appreciable effects of nTiO2 (up to 10 mg L−1) were observed in V. fischeri, Pseudokirchneriella subcapitata, Chydorus sphaericus, D. magna or Danio rerio (Velzeboer et al., 2008, Griffitt et al., 2008). Moreover, Wiench et al. (2009) examined the potential effects of nano-scale and non-nano-scale TiO2 on D. magna using three different test media, several pigment formulations – including coated nanoparticles – and a variety of preparation steps, and found little toxicity in their acute (48 h) toxicity tests (EC50 > 100 mg L−1). A similar conclusion was also reached in our recent study using D. rerio embryos, in which nTiO2 nanoparticles at concentrations as high as 500 mg L−1 did not show any toxic effects (Zhu et al., 2008). According to these studies, nTiO2 appears to exert no or low toxicity to eco-relevant species. However, the ecotoxicity tests in these studies were conducted using acute or short term exposure regimes. The long term and/or chronic effects of nTiO2 on aquatic organisms remain poorly defined. Interestingly, exposure of D. magna to 20 ppm nTiO2 for eight consecutive days was found to cause 40% mortality (Adams et al., 2006). In addition, nTiO2 at a concentration lower than 1.0 mg L−1 may cause respiratory toxicity and/or disturbances in the metabolism of some trace elements, such as Zn and Cu, in rainbow trout (Oncorhynchus mykiss) after 14 d of exposure (Federici et al., 2007). Moreover, the 21 d EC10 and EC50 values for reproductive effects of one coated nTiO2 on D. magna were 5 and 26.6 mg L−1, respectively (Wiench et al., 2009). Thus, the non-effect dose of nTiO2 in acute toxicity tests may still be toxic to aquatic organisms if delivered to these organisms for an extended period of time.

To further assess the ecological impact of nTiO2, and determine whether exposure time is an important parameter in evaluating nTiO2 toxicity to aquatic organisms, we conducted a comprehensive toxicity assessment of nTiO2 using D. magna as the test organism. This assessment included an acute test with extended exposure time from the traditional 48 h to 72 h as well as a 21 d chronic toxicity test. Furthermore, to better understand the mechanism of nTiO2 toxicity to D. magna, a detailed bioaccumulation profile of nTiO2 and its effects on the feeding behavior of D. magna were conducted. Considering that D. magna is at the base of the food chain in aquatic ecosystems, studying the relationship between the accumulation and the transportation of NPs within this organism and their chronic toxicity will offer important insights into the broad impact of NPs in aquatic environments.

Section snippets

Preparation and characterization of nTiO2 test solution

Uncoated, and powdered nanoscale Degussa P25 TiO2 (nTiO2), with an average surface area of 50 m2 g−1 and particle size of 21 nm, was obtained from Degussa (Essen, Germany). These P25 particles are comprised of 20% rutile and 80% anatase TiO2. A stock solution of 1.0 g L−1 nTiO2 was prepared by dispersing the nanoparticles in ultrapure water (Millipore, Billerica, MA, USA) with sonication for 10 min (50 W L−1 at 40 kHz); a further 10 min of sonication was conducted immediately before dosing each day.

nTiO2 characterization

Previous studies have shown that nTiO2 can aggregate in aquatic environments (Adams et al., 2006, Federici et al., 2007, Zhu et al., 2008). In the current study, we found that the addition of nTiO2 to the culture medium resulted in visible milk-white aggregates. Observed by SEM, these nTiO2 aggregates look like floccules with sizes from a few hundred nanometers to several microns in diameter (Fig. 1). Some of the aggregates were composed of strips of nTiO2 crystals (Fig. 1B). After detecting by

Discussion

Previous ecotoxicity studies with nTiO2 on D. magna often focused on exposure concentration, the physicochemical properties of nanoparticles, and NP pre-treatment. Hund-Rinke and Simon (2006) reported that nTiO2 (25 nm or 100 nm) concentrations of less than 3 mg L−1 exhibited little effect on the immobilization of daphnids, and the toxicity of nTiO2 under pre-illumination by simulated sunlight seemed to be higher than that of non-illuminated nTiO2. Lovern and Klaper (2006) reported a very high

Conclusion

Few aquatic ecotoxicity studies have focused on nTiO2, especially on the effects of prolonged exposure. Here, we reported the first comparative study of the acute and chronic toxicity of uncoated nTiO2 to D. magna. Our results demonstrated that the traditional 48 h acute toxicity test may not be sufficient for the toxicity assessment of nTiO2 because no or low toxicity was found within 48 h of exposure, but high toxicity was observed when the exposure time was extended to 72 h. Moreover, chronic

Acknowledgment

This study was supported by the US Environmental Protection Agency Science to Achieve Results Program (Grant # RD831713).

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