Toxicity of cerium and thorium on Daphnia magna

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Ce) (Cotton and Wilkinson, 1988; Huist, 1997). The exploitation of thorium .... nasi Puigdomenech from the Inorganic Chemistry of Royal In- stitute of Technology ...
Ecotoxicology and Environmental Safety 134 (2016) 226–232

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Toxicity of cerium and thorium on Daphnia magna Yuhui Ma a,1, Jingkun Wang b,1, Can Peng c, Yayun Ding a, Xiao He a, Peng Zhang a, Na Li a, Tu Lan a, Dongqi Wang a, Zhaohui Zhang c, Fuhong Sun d, Haiqing Liao d,n, Zhiyong Zhang a,n a Key Laboratory for Biological Effects of Nanomaterials and Nanosafety, Key Laboratory of Nuclear Radiation and Nuclear Energy Technology, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, China b Jiangsu Province Metallurgical Design Institute Co., Ltd, Jiangsu, 210007, China c School of public health, University of South China, Hunan, 421001, China d Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, China

art ic l e i nf o

a b s t r a c t

Article history: Received 21 January 2016 Received in revised form 1 September 2016 Accepted 2 September 2016

Cerium (Ce) and thorium (Th) are always thought to be chemically similar and have comparable toxic properties on living organisms. In the present study, the acute and chronic toxicity of these two elements to freshwater crustacean Daphnia magna were investigated in the modified reconstituted water (6 mg/L KCl, 123 mg/L MgSO4  7H2O, and 294 mg/L CaCl2  2H2O in Milli-Q water, pH 7.8). It seemed that Ce and Th had comparable acute toxicity on Daphnia: 24/48 h EC50 for Th and Ce were 7.3/4.7 μM and 16.4/ 10.7 μM, respectively. However, Ce was present as soluble ions while all of Th was present as particulate ThO2 in the exposure medium. Considering their different chemical forms and bioavailability, the toxic mechanisms of Ce3 þ and ThO2 on Daphnia would be totally different. To our knowledge, this is the first time to investigate the aquatic toxicity of thorium and cerium based on their actual chemical speciation in the exposure medium. The results also suggest that more attention should be paid on the detrimental effect of Th in the form of particulate ThO2. & 2016 Elsevier Inc. All rights reserved.

Keywords: Cerium Thorium Chemical speciation Acute toxicity Chronic toxicity Daphnia magna

1. Introduction Thorium is a naturally-occurring radioactive metal and is used as fuel in nuclear reactors to produce fissionable uranium isotopes. Monoisotopic 232Th, emitting α-(90%), β-(1%), and γ-(9%) rays with a half-life of 1.4  1010 years. Concentrations of Th in natural water sources was reported to vary over a widely range. For instance, surface and groundwater exhibited low Th concentration in the range of 0.009–2.9 μg/L, but Th in the contaminated water was in the range of 800–1400 μg/L (3.3–5.8 Bq/L) in southeastern Brazil (Veado et al., 2006). Thorium is a typical lipophilic element and its geochemical behavior is very similar to the lanthanides (especially Ce) (Cotton and Wilkinson, 1988; Huist, 1997). The exploitation of thorium containing mineral resources and growing industrial uses of Th imply increasing concentrations of this element in the environment, especially in the aquatic environment. However, little research emphasis has been placed on the toxicity of Th to aquatic organisms. Authors from Brazil investigated the biochemical and cytogenetic alteration in the silver catfish when exposed to different concentrations of Th (Correa n

Corresponding authors. E-mail addresses: [email protected] (H. Liao), [email protected] (Z. Zhang). 1 These authors contributed equally to this work. http://dx.doi.org/10.1016/j.ecoenv.2016.09.006 0147-6513/& 2016 Elsevier Inc. All rights reserved.

et al., 2008; Kochhann et al., 2009). The alterations in the oxidative parameters of silver catfish gills were correlated with Th accumulation in this organ. The decrease of glutathione-S-transferase (GST) and SOD activity and increase of lipid peroxidation (LPO) exposed to 747.2 μg/L Th (3.22 μΜ) suggested that oxidative damage occurred in the gills. It has been thought that the chemical toxicity of Th may be similar to its stable chemical analogue Ce, but the ionizing activity associated with radioactive decay of 232Th can result in additional toxic effects on an organism. Evseeva et al. (2010) determined the toxicity of 232Th and Ce (III) to the freshwater green alga Chlorella vulgaris. They found that based on EC50 and regression equation parameters, Th was more toxic to C. vulgaris after a 24-h exposure than Ce. In contrast, no-observableeffect concentration (NOEC) and lowest observable-effect concentration (LOEC) values for Th were similar to those for Ce. Although Ce was one of the most studied lanthanide (Ln) elements and progress has been made in understanding Ce toxicity to different plant (Diatloff et al., 2008) and animal (Huang et al., 2010; Kawagoe et al., 2005) species, a very limited number of studies on their effects on aquatic biota. The toxic effects of Ce to Elodea canadensis were shown as a reduction in photosynthetic pigments, disruption of nutrient elements, modulating antioxidant enzymes, and increases in malondialdehyde (MDA) content (Chu et al., 2014). The results of Paoli et al. (2014) showed that treatment with Ce solutions induces Ce extra- and intra-cellular bioaccumulation,

Y. Ma et al. / Ecotoxicology and Environmental Safety 134 (2016) 226–232

which in turn causes an acute toxicity, evident as decreased sample viability, marked decrease in the photosynthetic performance and important changes in the ultrastructure of the lichen Xanthoria parietina. All of the above studies have advanced our understanding of biological effects on various species for thorium and cerium. However, Th and Ce induced toxic effects on aquatic crustacean organisms (for example, Daphnia) have not been demonstrated so far. Moreover, Th4 þ and Ce3 þ are highly charged cations, so they tend to interact with anions (e.g. phosphate, carbonate, etc.) and form insoluble precipitates in aqueous solutions (Clark et al., 1995; Liu and Byrne, 1997). Consequently, toxicity and bioavailability of Th and Ce can be significantly altered. Unfortunately, no detailed studies on this aspect have been carried out as yet. The present work aimed to investigate the acute (24 and 48 h) and chronic toxicity (21 d) of Th and Ce to Daphnia magna based on their chemical speciation in the exposure medium.

2. Materials and methods 2.1. Test organisms Daphnia magna (D. magna) were obtained from cultures maintained at the Research Center for Eco-Environmental Sciences (Chinese Academy of Sciences) and have been maintained in our laboratory for more than one year. They were cultured in large beakers with moderately hard reconstituted water in a climate chamber at 2072 °C with a 16 h light/8 h dark photoperiod. D. magna were fed with a suspension of the freshwater unicellular Chlorella vulgaris at a concentration of 105–106 cell/ml once daily. All the animal experiments were conducted in accordance with the protocols approved by the Ethics Committee of Animal Care and Experimentation of the National Institute for Environmental Studies, China. 2.2. Materials and test media Th and Ce were used in the form of Th(NO3)4  4H2O and Ce (NO3)3  6H2O, with purity over 99%. All chemicals were analytical grade and purchased from Beijing Chemical Plant (China). According to Organization for Economic Cooperation and Development (OECD) Guideline 202 (OECD, 2004), some media containing chelating agents, such as M4 and M7 media, should be avoided for testing substances containing metals. To control the physicochemical condition of the water during the exposure, we adopted reconstituted water (RW, 64.8 mg/L NaHCO3, 5.8 mg/L KCl, 123 mg/L MgSO4  7H2O, and 294 mg/L CaCl2  2H2O in Milli-Q water) as the test medium in this study, with the pH being adjusted to 7.8. However, preliminary experimental results showed that insoluble precipitates of cerium and thorium could be formed induced by NaHCO3 in the medium. Therefore, NaHCO3 was replaced by NaOH to adjust the pH value and avoid precipitation, which was called modified reconstituted water (MRW). The survival, growth and reproduction of D. magna were not affected in this medium. Test solutions were diluted from a stock solution of Ce(NO3)3  6H2O or Th(NO3)4  4H2O to reach the corresponding nominal concentrations in the acute toxicity experiment in RW and MRW media, respectively. The measured concentrations of Ce or Th in the two kinds of media at 0 h (the start of test) and 48 h (the end of the test) were determined by ICP-MS (acidification with 2% HNO3) after centrifugation (11,000 rpm for 10 min) and filtration (0.22 mm filter). The insoluble forms of Th group in MRW at 48 h was thoroughly washed with ultrapure water and characterized by SEM (Hitachi, S-4800) with EDX, and XRD (Bruker D8), respectively.

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2.3. MEDUSA program To make equilibrium diagrams of different cerium and thorium chemical forms present in the MRW medium, sophisticated algorithms (MEDUSA program) were used for the construction of distribution diagrams. The basic parameters, including equilibrium constants that are necessary for the calculation of distribution diagrams are in the program database. The program author is Ignasi Puigdomenech from the Inorganic Chemistry of Royal Institute of Technology, Stockholm, Sweden (Puigdomenech, 2010). 2.4. Acute Toxicity Acute toxicity testing was directed by the OECD protocol 202 Daphnia sp. Acute Immobilization Test (2004). D. magna neonates (o24 h old) of third to six offspring born by a single parthenogenic female were placed in test solutions. To verify organism sensitivity, acute tests with the reference compound potassium dichromate were performed at least twice a year. Stock solutions of each metal were prepared in Milli Q water and exposure concentrations of them were prepared by diluting stock solution in the MRW medium. The nominal concentrations of Th were 0, 0.43, 2.2, 4.3, 8.6, 21.6, 43.1 μM and Ce were 0, 0.71, 3.6, 7.1, 14.3, 35.7, 71.4 μM, respectively. Test beakers contained 50 ml of media and 8 daphnias and each treatment was replicated three times. Test solutions were not renewed and organisms were not fed during the 48-h exposure period. After the experiment, D. magna that were not showing any sign of motion even after gentle agitation of the container were thought immobile. Immobility data were recorded during an exposure period of 24 and 48 h, which were allowed to determine EC50 of the two metals using Probit analysis (Finney, 1978). 2.5. Chronic toxicity The MRW medium was chosen for 21 d chronic toxicity test to avoid precipitation in accordance with OECD guideline 211 (OECD, 2012). The requirement of D. magna was as described for the acute bioassays. Based on the requirement that the maximum concentration should below LC50 of acute toxicity, we set seven nominal concentrations for Th (0, 0.043, 0.086, 0.22, 0.43, 0.86, and 1.72 μM) or Ce (0, 0.071, 0.14, 0.36, 0.71, 1.43, and 2.86 μM), with each treatment replicated eight times. A single neonate daphnia (o24 h old) was raised in each beaker containing 25 ml test solution. The animals were transferred to fresh test solutions with additional algae (1  105 cell/ml) being added every second day. Each test was terminated either when all control females fulfilled their third brood or at 21 d. The number of neonates and age of D. magna at the release of first-, second-, and third-brood eggs were recorded and analyzed. The exuviaes were removed from media every other day and then mounted on a microscope glass slide using glycerol. The growth was assessed by measuring the size of non-extensible pieces of the exuviae (the length of the antenna’s first segments) using an optical microscope (Auffan et al., 2013). 2.6. Data statistical analysis Data were expressed as mean 7 standard deviation. Mortality was analyzed and EC50 was calculated using a probit method. OneWay ANOVA analysis was employed to compare the significant difference between treatments and controls. Po 0.05 was considered to be a significant difference. The lowest-observable-effect concentration (LOEC) and no-observable-effect concentration (NOEC) were calculated using Dunnett’s test. All statistical analyses were conducted using Statistical Packages for the Social

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Sciences (SPSS) Version 17.0.

3. Results 3.1. Chemical speciation of Ce and Th in the media The compositions of exposure media play a key role in ecotoxicology studies of the lanthanides and actinides because of the formation of “insoluble species” with specific ligands in most of artificial media. As shown in Fig. 1A, the measured concentrations of Ce in the RW medium were close to nominal ones up to 7.14 μM and then reached a plateau. At the highest concentration (71.4 μM), less than 20% and 15% of nominal Ce was detected at the beginning (0 h) and the end (48 h) of the experiment, respectively. Moreover, the precipitation in RW medium at 48 h can be observed by naked eyes (Fig. S1A). Given the high concentration of NaHCO3 in RW, the rapid loss of cerium from the medium might be due to the precipitation with carbonates. Therefore, NaHCO3 was replaced by NaOH to adjust pH value, which was called MRW medium. In this medium, the solution containing Ce3 þ ions was transparent (Fig. S1A) and the measured Ce concentrations were very close to nominal ones at the beginning, and the decrease of soluble forms after 48 h was less than 15% (Fig. 1A). But for Th, the solutions were both slightly cloudy either in the RW or MRW medium (Supplementary data, Fig. S1B). The measured concentration was only about 20% of that nominal one at the highest concentration even in the MRW medium (Fig. 1B). After added Ce or Th, owing to the hydrolysis reaction, the pH values of MRW solutions were changed from 7.8 to 6.8 and 6.3 at 0 h, respectively.

At the end of acute experiment (48 h), the changes of pH value were both less than 0.2 pH units of the two kinds of solutions. The survival, growth and reproduction of D. magna were not affected by these pH values based on the report of Zhuang (1994). Considering the complexity of exposure solutions, we calculated the distribution diagrams of different chemical forms of Ce and Th at the highest concentration present in the MRW medium using the MEDUSA program. As can be seen from Fig. 1C, the concentration of free Ce3 þ ions decreases with the increasing pH value due to the formation of hydroxo-complexes (CeOH3 þ and Ce (OH)2 þ ), and there was no soluble Ce present in solutions because of the formation of Ce(OH)3 precipitation at the pH value over 10. In this study, Ce was mainly present as free Ce3 þ and soluble CeSO4 þ ions, as well as a small amount of CeOH2 þ in the MRW medium (pH 6.8), which was consistent with the measured concentrations (Fig. 1A). In contrast, there were no any free Th4 þ ions in the MRW medium (pH 6.3), and all of Th was present as crystalline ThO2 (Fig. 1D). The insoluble forms in the Th-containing group after 48 h were characterized by SEM and EDX. As shown in Fig. 2A and B, the sediment was nanoscale particles and the presence of Th was verified by the EDX spectrum. Further, the sediment was characterized by XRD (Fig. 2C). All of the broadening diffraction peaks in the pattern can be indexed to the cubic structure of ThO2 (JCPDS 42-1462). No other diffraction peaks indicated the product is of pure phase. Thus, the results of the experiment and theoretical calculation were corroborated each other and confirmed that Th was indeed in the form of particulate ThO2 in the MRW medium.

Fig. 1. Nominal and measured Ce (A) and Th (B) concentrations in the RW (triangle) and MRW (circle) media for 0 h and 48 h. Distribution diagram of different forms of Ce (C) and Th (D) at the highest treated concenteration in dependence on pH values. [SO42-]TOT ¼ 0.5 mM, [Cl-]TOT ¼ 4.08 mM, [Mg2 þ ]TOT ¼ 0.5 mM, [K þ ]TOT ¼ 83.9 μM, [Ca2 þ ]TOT ¼ 2.0 mM, [Na þ ]TOT ¼24.0 μM, [Ce3 þ ]TOT ¼ 71.4 μM, or [Th4 þ ]TOT ¼43.1 μM.

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Fig. 2. SEM image (A), EDX spectrum (B), and XRD pattern (C) of the sediment in the Th group.

Therefore, the toxicity of particulate Th and ionic Ce to D. magna cannot be compared directly under this condition.

3.2. Acute toxicity D. magna is crustacean and always be used as a model organism in aquatic toxicology and ecotoxicology studies. The mortality percentages at different concentrations of Th and Ce in acute toxicity are shown in Fig. S2. The 24- and 48-h EC50 of Th and Ce to D. magna in the MRW medium are calculated and summarized in Table 1. 24 and 48-h EC50 values for Th were 7.3 and 4.7 μM, while those for Ce were 16.4 and 10.7 μM, respectively. It seemed that Th was more toxic than Ce to D. magna in terms of their EC50 values. However, the bioavailability and uptake route of the particulate form of metals may totally be different from the aqueous one for aquatic organisms and the mechanism need further study. Table 1 The 24-h and 48-h EC50 of Th and Ce to D. magna in acute toxicity bioassay with 95% confidence interval (CI).

Th(IV) Ce(III)

24-h EC50 (μM) (95% CI)

48-h EC50 (μM) (95% CI)

7.3 (5.8  9.2) 16.4 (13.2  20.8)

4.7 (3.2  6.6) 10.7 (8.6  13.4)

3.3. Chronic toxicity Similar to that in acute toxicity, Ce was also present as soluble ions while Th was as crystalline ThO2 in the MRW medium at the lowest and highest concentrations for the chronic toxicity (Fig. S3). Although Th and Ce both caused significant mortality to D. magna at the highest concentration, there were at least three animals survived for each group at the end of the experiment. There was no effect of Th on the mean brood size per living parent at the concentrations less than 0.22 μM. However, the average number of neonates of the three broods significantly decreased at concentrations of 0.86 μM (p o0.05 for the first-brood and p o0.01 for the second- and third-brood) and 1.72 μM (p o0.01) of Th exposure, and that of the third-brood also obviously decreased at 0.43 μM of Th compared with the control (po 0.01, Fig. 3A). Ce had similar inhibition on the offspring production at higher concentrations (Fig. 3B). The ages of all the three broods for D. magna were significantly delayed when exposed to 1.72 μM of Th, which was postponed for

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Fig. 3. Effect of Th (A) and Ce (B) on mean number of brood neonates per living parent D. magna. Significant difference of each experimental value compared with the control was marked with ‘‘asterisk’’ (p o0.05) or ‘‘double asterisk’’ (p o0.01).

Fig. 4. Effect of Th (A) and Ce (B) on age at reproduction of brood neonates of D. magna. Significant difference of each experimental value compared with the control was marked with ‘‘asterisk’’ (p o 0.05).

more than 3 days compared with the control (p o0.05). In addition, 0.43 and 0.86 μM of Th also caused significant delays to the third brood of D. magna (p o0.05, Fig. 4A). In contrast, there was no significant influence on ages of the three broods for Daphnia at all the concentrations of Ce exposure (Fig. 4B). For growth, the most significant effects were observed at the highest concentration of both the Th and Ce exposure (po 0.05). The lengths of the first segments of the antenna, the non-

extensible pieces of the D. magna exuviaes, were reduced by 21.5%, 22%, and 25.2% for Th, as well as by 27.8%, 25.7%, and 15.6% for Ce with respect to each control at the highest concentration in the first-, second-, and third-reproductive instars, respectively (Fig. 5). Moreover, the length of the first segments of the antenna of the exuviae of D. magna was also shortened by Th at 0.86 μM (p o0.05, Fig. 5A). Based on these results, the LOEC and NOEC values of Th and Ce

Fig. 5. Effect of Th (A) and Ce (B) on the first segment lengths of the antenna of the brood exuviaes of D. magna. Significant difference of each experimental value compared with the control was marked with ‘‘asterisk’’ (p o 0.05).

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Table 2 Chronic toxicity of Th and Ce to D. magna. LOEC (μM)

Clutch size Age at reproduction Length of the antenna

NOEC (μM)

Th (IV)

Ce (III)

Th (IV)

Ce (III)

0.43 0.43 0.86

0.72 – 2.86

0.22 0.22 0.43

0.36 – 1.43

-: Not determined.

on chronic toxicity to D. magna were determined and listed in Table 2. The minimum effective concentrations of Th and Ce were 0.43 and 0.72 μM, respectively, indicating that the offspring production is the most sensitive index among the three endpoints.

4. Discussion Solubility and bioavailability of lanthanides and actinides are influenced by many factors, such as pH, concentration and type of ligands, and temperature, etc. Therefore, the composition of artificial exposure media potentially plays a key role when attempting to determine the toxicity of them. The nitrates, chlorides, and sulfates of lanthanides are soluble, while their carbonates, phosphates, and hydroxides are insoluble (Johannesson et al., 1996; Liu and Byrne, 1997; Wells and Wells, 2000) [8, 10, 15]. Similarly, Th4 þ ions tend to form hydrolyzed species and/or insoluble residues in aqueous solutions (Clark et al., 1995). Moreover, the formation of colloidal species of this element is known to start at very low pH (Cornelis et al., 2005). In the RW medium in this study, the percentages of Ce and Th remained in filterable forms were very small at the beginning of the tests and decreased with time (Fig. 1A and B), which was probably caused by the formation of carbonate complexes. However, rare earth carbonate precipitates are highly insoluble, with solubility products between 10  35 and 10  29 (Firsching and Mohammadzadei, 1986), while the precipitate of thorium carbonate might be dissolved through formation of carbonate complex [Th (CO3)5]6- at higher concentrations of carbonate (Felmy et al., 1997; Joao et al., 1995). The morphology and quantity of precipitates were both different in the two kinds of solutions (Supplementary data, Fig. S1). In order to compare the aquatic toxicity of the two elements under the similar chemical speciation composition, we adopted the MRW medium without carbonate. But unfortunately, the filterable forms of Th were still very low in this medium (Fig. 1B). Further, we calculated the chemical forms of them in the MRW medium using the MEDUSA program. The actual species for Ce were mainly Ce3 þ and CeSO4 þ ions, and for Th was ThO2 in the exposure medium (Fig. 1C and D). The results of SEM and XRD also confirmed that Th was in the form of particulate ThO2 in this medium (Fig. 2). It has been reported that logKsp value for ThO2  xH2O was 45.9 70.5 and the minimum solubility of fully crystalline ThO2 (above pH 6) was only 10  9.6 M (Ryan and Rai, 1987), which means the solubility of ThO2 in the water was extremely low. However, a small amount of Th in the supernatant after filtration was measured by ICP-MS (Fig. 1B), which might be due to some tiny ThO2 particles passing through the filter and being ionization by the ICP torch. All in all, a detailed consideration of metal speciation during exposure was essential to understand the ecotoxicity of lanthanides and actinides to aquatic organisms. To assess the toxicity of Th and Ce over a wide range of concentrations, EC50 values of them to the freshwater crustacean D. magna were determined in RMW medium. Regardless of their forms in the solution, Th and Ce had comparable acute toxicity in terms of 24 and 48 h EC50 values (Table 1). For chronic toxicity, the

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reproduction of D. magna was far more sensitive than the acute tests, showing effects at 10-fold lower concentrations than effects on mortality. The extent of inhibition on clutch size (Fig. 3) and the first segment lengths of the antenna (Fig. 5) at higher doses were both similar under the two treatments. In contrast, the ages of the release of broods were not obviously postponed under the exposure of Ce, while there were 3-to-4-d delays in the release of the three broods compared to the control at the dosage of 400 μg Th/L (Fig. 4). It is established that at a given food level, clutch size will primarily be determined by body length and instar duration (Green, 1956). By increasing the inter-moult period, the Daphnias have more time to accumulate resources which can subsequently be allocated to reproduction. This comes at a cost as it increases the age at maturity and decreases the maximum rate of reproduction (Snell, 1978). It should be noted that Ce was present as soluble ions, but Th as insoluble forms in the exposure medium. Accordingly, the toxic mechanisms of soluble Ce3 þ and insoluble ThO2 on living organisms would be totally different (Fritsch, 1999). There are several potential mechanisms by which the Ln may exert toxicity on aquatic organisms, however, the exact mode of interaction remains unknown. Ln3 þ have an ionic radius very close to that of Ca2 þ (  1Ǻ) (Evans, 1990), which make them preferentially bound to calcium binding sites (Das et al., 1988), It had been reported that Daphnia actively absorbed calcium during each moult cycle to harden the carapace (Porcella et al., 1969). Ce may promote the displacement or replacement of calcium causing interference with the normal moult cycle of Daphnia. As a radioactive element, Th may exert radiological toxicity on D. magna because it is a long lived naturally occurring radionuclide and α-, β- and γ-emitter. Ionizing radiation energy may cause water molecules ionization and free radicals formation that may enhance the adverse effect of Th and its daughter decay products on D. magna. In addition, the main route of Th uptake in D. magna might be via the carapace, and ThO2 adsorbed onto the carapace could be considered as emitters with high linear energy transfer. In the present study, 24h and 48-h EC50 (7.3 and 4.7 μM) corresponded to 232Th activity concentrations in water of 6.9 Bq/L and 4.4 Bq/L, respectively. These activity concentrations can be used to calculate radiation dose rates to zooplankton, through the application of appropriate exposure dosimetric models such as those provided within the ERICA Tool (Brown et al., 2008). According to the implementation of concentration factors and dose conversion factors in this particular tool, the risk quotients (RQs) are both o1 at the above two activity concentrations, indicating that there is a very low probability that the assessment dose rate to any organism exceeds the incremental screening dose rate and therefore the environmental risk can be considered negligible. It has been reported that precipitation of lanthanides in artificial media may induce a marked underestimation of the ecotoxicity of these elements. For example, in the TW media with the lowest carbonate hardness, the 48-h EC50 of lanthanum (La) was 43 μg/L, while that was 1180 μg/L in the ASTM standard media (Barry and Meehan, 2000), indicating that the exposure medium was one important factor in determining the toxicity of La to Daphnia. In another study with D. magna, Lürling and Tolma (Lürling and Tolman, 2010) did not find toxic effects after 1000 μg/ L La exposure in phosphorous-free medium, where most of La would have formed inorganic complexes with anions and a low concentration of free La3 þ remained. In these studies, precipitations of Ln compounds were considered to be biologically inert. However, recent developments of nanotoxicology suggest that some fine particles can also exert adverse effects on organisms. Our previous study indicates that CeO2 nanoparticles (c.a. 8.5 nm) could induce ROS accumulation and oxidative damage in C.

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elegans, and finally lead to a decreased lifespan at environmental relevant concentrations (1–100 nM) (Zhang et al., 2011). It is resonable to postulate that particulate ThO2 could exhibit toxic effects to aquatic organisms via an unknown mechanism.

5. Conclusions The results of our study demonstrated that compositions of test media significantly affect the chemical speciation of lanthanides and actinides. In the MRW medium without NaHCO3, Ce was present as soluble ions, while all of Th was present as particulate ThO2. Considering their different bioavailability and chemical reactivity, the toxicity of Th and Ce to D. magna cannot be compared directly and Ce is not a toxicological analogue of Th under specific conditions. Further studies are needed to characterize the mechanism involved in the induction of toxicity by insoluble forms of Th.

Acknowledgements This work was financially supported by the Ministry of Science and Technology of China (Grant nos. 2011CB933400, 2013CB932703), Ministry of Environmental Protection of China (Grant no. 201209012), and Project 11275215, 11275218, 11375009, and 11575208 supported by National Natural Science Foundation of China.

Appendix A. Supplementary material Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/j.ecoenv.2016.09.006.

References Auffan, M., Bertin, D., Chaurand, P., Pailles, C., Dominici, C., Rose, J., Bottero, J.-Y., Thiéry, A., 2013. Role of molting on the biodistribution of CeO2 nanoparticles within Daphnia pulex. Water Res 47, 3921–3930. Barry, M.J., Meehan, B.J., 2000. The acute and chronic toxicity of lanthanum to Daphnia carinata. Chemosphere 41, 1669–1674. Brown, J., Alfonso, B., Avila, R., Beresford, N.A., Copplestone, D., Pröhl, G., Ulanovsky, A., 2008. The ERICA tool. J. Environ. Radioact. 99, 1371–1383. Chu, W.Y., Cai, S.J., Fu, Y.Y., Li, F.F., Xu, T., Qiu, H., Xu, Q.S., 2014. The toxicity of cerium nitrate to Elodea canadensis: subcellular distribution, chemical forms and physiological effects. Acta Physiol. Plant. 36, 2491–2499. Clark, D.L., Hobart, D.E., Neu, M.P., 1995. Actinide carbonte complexes and their importance in actinide environmental chemistry. Chem. Rev. 95, 25–48. Cornelis, R., Caruso, J., Crews, H., Heumann, K., 2005. Handbook of Elemental Speciation II: Species In The Environment, Food, Medicine And Occupational Health. Wiley Online Library, UK. Correa, L.M., Kochhann, D., Becker, A.G., Pavanato, M.A., Llesuy, S.F., Loro, V.L., Raabe, A., Mesko, M.F., Flores, É.M., Dressler, V.L., 2008. Biochemistry, cytogenetics and bioaccumulation in silver catfish (Rhamdia quelen) exposed to different thorium concentrations. Aquat. Toxicol. 88, 250–256. Cotton, F., Wilkinson, G., 1988. Advanced Inorganic Chemistry. Pub. Wiley

Interscience, New York, pp. 156–157. Das, T., Sharma, A., Talukder, G., 1988. Effects of lanthanum in cellular systems. Biol. Trace Elem. Res. 18, 201–228. Diatloff, E., Smith, F., Asher, C., 2008. Effects of lanthanum and cerium on the growth and mineral nutrition of corn and mungbean. Ann. Bot. 101, 971–982. Evans, C., 1990. Biochemistry of the Lanthanides. Plenum Press, New York. Evseeva, T., Geras’kin, S., Majstrenko, T., Brown, J., Belykh, E., 2010. Comparative estimation of 232Th and stable Ce (III) toxicity and detoxification pathways in freshwater alga Chlorella vulgaris. Chemosphere 81, 1320–1327. Felmy, A.R., Rai, D., Sterner, S.M., Mason, M.J., Hess, N.J., Conradson, S.D., 1997. Thermodynamic models for highly charged aqueous species: Solubility of Th (IV) hydrous oxide in concentrated NaHCO3 and Na2CO3 solutions. J. Solut. Chem. 26, 233–248. Finney, D.J., 1978. Statistical Method in Biological Assay, 3rd ed. Griffin, Weycombe, UK, London. Firsching, F.H., Mohammadzadei, J., 1986. Solubility products of the rare-earth carbonates. J. Chem. Eng. Data 31, 40–42. Fritsch, C.L., P., 1999. Chemical toxicity of some actinides and lanthanides towards alveolar macrophages: an in vitro study. Int. J. Radiat. Biol. 75, 1459–1471. Green, J., 1956. Growth, size and reproduction in Daphnia. (Crustace.: Cladocera), Proc. Zool. Soc. Lond., 173–204. Huang, S.F., Li, Z.Y., Wang, X.Q., Wang, Q.-X., Hu, F.-F., 2010. Cerium caused life span shortening and oxidative stress resistance in Drosophila melanogaster. Ecotoxicol. Environ. Saf. 73, 89–93. Huist, W., 1997. Thorium. Gmelin Handbook of Inorganic and Organometallic Chemistry, supplement v.B1, eighth ed. Springer-Verlag, Berlin, Heidelberg. Joao, A., Burrows, H., Zikovsky, L., Lipponen, M., 1995. Study of thorium and cerium carbonate complexes. Determination of the stability constants of pentacarbonatothorate (IV) and dicarbonatocerate (IV) ions, at pH 8.8. Radiochim. Acta 68, 177–183. Johannesson, K.H., Stetzenbach, K.J., Hodge, V.F., Berry Lyons, W., 1996. Rare earth element complexation behavior in circumneutral pH groundwaters: assessing the role of carbonate and phosphate ions. Earth Planet. Sci. Lett. 139, 305–319. Kawagoe, M., Hirasawa, F., Cun Wang, S., Liu, Y., Ueno, Y., Sugiyama, T., 2005. Orally administrated rare earth element cerium induces metallothionein synthesis and increases glutathione in the mouse liver. Life Sci. 77, 922–937. Kochhann, D., Pavanato, M.A., Llesuy, S.F., Correa, L.M., Konzen Riffel, A.P., Loro, V.L., Mesko, M.F., Flores, É.M., Dressler, V.L., Baldisserotto, B., 2009. Bioaccumulation and oxidative stress parameters in silver catfish (Rhamdia quelen) exposed to different thorium concentrations. Chemosphere 77, 384–391. Lürling, M., Tolman, Y., 2010. Effects of lanthanum and lanthanum-modified clay on growth, survival and reproduction of Daphnia magna. Water Res. 44, 309–319. Liu, X., Byrne, R.H., 1997. Rare earth and yttrium phosphate solubilities in aqueous solution. Geochim. Cosmochim. Acta 61, 1625–1633. OECD, 2004. OECD Guidelines for the Testing of Chemicals. ‘Daphnia sp., acute immobilisation test. OECD, 2012. OECD Guidelines for the Testing of Chemicals. ‘Daphnia magna Reproduction test. Paoli, L., Fiorini, E., Munzi, S., Sorbo, S., Basile, A., Loppi, S., 2014. Uptake and acute toxicity of cerium in the lichen Xanthoria parietina. Ecotoxicol. Environ. Saf. 104, 379–385. Porcella, D.B., Rixford, C.E., Slater, J.V., 1969. Molting and calcification in Daphnia magna. Physiol. Zool., 148–159. Puigdomenech, I., 2010. Program MEDUSA (Make equilibrium diagrams using sophisticated algorithms). Royal Institute of Technology. Inorg. Chem., 10644. Ryan, J.L., Rai, D., 1987. Thorium (IV) hydrous oxide solubility. Inorg. Chem. 26, 4140–4142. Snell, T.W., 1978. Fecundity, developmental time, and population growth rate. Oecologia 32, 119–125. Veado, M., Arantes, I., Oliveira, A., Almeida, M., Miguel, R., Severo, M., Cabaleiro, H., 2006. Metal pollution in the environment of Minas Gerais State–Brazil. Environ. Monit. Assess. 117, 157–172. Wells Jr, W., Wells, V.L., , 2000. The lanthanides, rare earth metals. Patty's Toxicology. Zhang, H., He, X., Zhang, Z., Zhang, P., Li, Y., Ma, Y., Kuang, Y., Zhao, Y., Chai, Z., 2011. Nano-CeO2 exhibits adverse effects at environmental relevant concentrations. Environ. Sci. Technol. 45, 3725–3730. Zhuang, D., 1994. The effects of low pH value on survival, growth and reproduction of Daphnia magna (in Chinese). China. Environ. Sci. 14, 107–111.