Effects of Carbon Nanotubes, Chars, and Ash on Bioaccumulation of

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Effects of Carbon Nanotubes, Chars, and Ash on Bioaccumulation of Perfluorochemicals by Chironomus plumosus Larvae in Sediment Xinghui Xia,*,† Xi Chen,† Xiuli Zhao,† Huiting Chen,† and Mohai Shen† †

School of Environment, Beijing Normal University/State Key Laboratory of Water Environment Simulation, Beijing, 100875, China S Supporting Information *

ABSTRACT: This study examined the effect of five types of carbonaceous materials (CMs) in sediment on bioaccumulation of perfluorochemicals (PFCs) by Chironomus plumosus larvae. The CMs included two multiwalled carbon nanotubes (MWCNT10 and MWCNT50), maize straw- and willow-derived chars, and maize straw-origin ash. The PFCs included perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA), perfluorononanoic acid (PFNA), perfluorodecanoic acid (PFDA), perfluoroundecanoic acid (PFUnA), and perfluorododecanoic acid (PFDoA). The CMs with different concentrations (0−1.5% dry weight) were amended into sediments spiked with PFCs and aged for 60 d. The uptake rate constants (ks) for each PFC to larvae differed with different CM amendments (p < 0.05), while elimination rate did not change significantly (p > 0.05). Decreasing PFC concentration in larvae (CB) was found with increasing CM concentration (f CM) in the sediments, and a linear positive correlation existed between 1/CB and f CM (p < 0.05). The effect of CMs on PFC bioaccumulation agreed well with the CM properties; MWCNT10 with the highest specific surface area resulted in the lowest ks values and biota−sediment accumulation factors (BSAF), with a BSAF reduction of 66%− 97% by a 1.5% amendment. The mechanism was explored by analyzing the aqueous phase concentrations of PFCs and the sorption of PFCs on sediments amended with CMs. The results suggested that the decreasing trend of PFCs in larvae was caused by the decreasing aqueous phase concentration with increasing CM concentration. In the studied conditions with low PFC concentrations, the bioaccumulation of PFCs was a linear partitioning between pore water and biota, and the sorption of PFCs to the sediment/CM mixtures was a two domain linear distribution. This study suggests that both the type and concentration of carbonaceous materials in sediment can affect the bioaccumulation of PFCs to benthic organisms through changing their aqueous phase concentrations.

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INTRODUCTION Perfluorinated compounds (PFCs) are a group of chemicals that have attracted increasing attention in recent years. They have been widely used for over 50 years in industrial and consumer products, including protective coatings for textiles, furniture, and paper products.1 PFCs have been detected in water,2−4 sediment,5,6 and aquatic organisms.7,8 Recent studies indicate that PFCs can accumulate in sediment via sorption,9,10 and sediment may be an important source of PFCs for benthic biota.11 In addition, PFCs are environmentally persistent and potentially harmful pollutants; toxicological studies have demonstrated that the most two prevalent PFCs in the environment, perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA), may induce liver toxicity, reproductive toxicity, developmental toxicity, and potential carcinogenicity on test organisms.12,13 Therefore, bioavailability of PFCs in sediment to benthic biota is a significant environmental concern. Carbon nanotubes (CNTs) and black carbon (BC), two carbonaceous materials (CMs), can reduce the bioavailability of hydrophobic organic compounds (HOCs) in soils and sediments due to their extensive sorption capacity. For example, soot has very high affinities for polycyclic aromatic © 2012 American Chemical Society

hydrocarbon (PAHs) and polychlorinated biphenyls (PCBs) and it can lower aqueous concentrations of the contaminants, leading to a reduction of the potential uptake by aquatic organisms. 14,15 Presence of CNTs in sediments could significantly reduce the bioaccumulation of PAHs, PCBs, and polybrominated diphenyl ethers (PBDEs) in benthic invertebrates.16,17 So far, studies about the effects of carbonaceous materials on the bioaccumulation of HOCs in sediment have mainly covered PAHs, PCBs, and PBDEs. For PFCs, although there is much study of PFC concentrations in aquatic organisms,18,19 little work has been reported on the bioaccumulation potential of PFCs from sediments,20 and no research has been reported about the effects of carbonaceous materials on bioaccumulation of PFCs. BC is ubiquitous in environment; with sharp increases in the application and use of CNTs, it can be expected that increasing amounts of CNTs will be released into environment. Therefore, it is necessary to study the effects of both CNTs and Received: Revised: Accepted: Published: 12467

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Table 1. Characteristics of Carbon Nanotubes, Chars, and Ash elemental composition (%) adsorbent W400 M400 MA adsorbent MWCNT10 MWCNT50

C

H

73.1 4.46 66.6 4.09 11.2 3.76 outer diameter (nm) 10−20 >50

C/H

BET surface area (m2 g−1)

N

1.37 0.486 1.36 1.68 0.25 1.32 length purity (μm) (%) 10−30 10−20

>95 >95

7.21 11.6 38.3 heavy metals (‰)

micropore area (m2 g−1)

12.1 BET surface area (m2 g−1)

0.92 0.62

324.9 97.2

meso- and macropore area (m2 g−1)

micropore area (m2 g−1)

26.2 meso- and macropore area (m2 g−1)

32.5 19.9

292.4 77.3

pHzpc 2.3 2.2 10.5 pHzpc 3.2 3.5

nium (TBA) hydrogen sulfate and HPLC grade methyl tertbutyl ether (MTBE) were obtained from Acros Organics. All of the solvents used in this study were of chromatography grade, and other chemicals were of analytical grade. Multiwalled carbon nanotubes (MWCNT10 and MWCNT50) synthesized by the chemical vapor deposition method were supplied by Beijing Nachen S&T Co., Ltd., China; the numbers after MWCNT are their outer diameters (nm) (Table 1). Chars were prepared by pyrolysis of maize (Zea mays) straw and willow (Salix babylonica) sawdust according to Glaser et al.26 and Braida et al.27 They were separately put into porcelain crucibles, covered with a fitted lid, and heated isothermally under oxygen-limited conditions in a preheated muffle furnace at 400 °C for 2h. The maize strawand willow-derived chars were labeled as M400 and W400, respectively. Ash was derived from maize straw and is referred to here as MA. To produce ash, maize straw was burned on a stainless steel plate (1 m × 1 m) in air under uncontrolled conditions.28 The chars and ash were gently ground and passed through a 0.15-mm nylon sieve. Then the carbon nanotubes, chars, and ash were characterized (detailed procedure see the SI), and the parameters of CMs are shown in Table 1. Sediment with nondetectable levels of PFCs was collected from the upstream of the Yongding River (N 40°01′06″, E 115°50′26″) of China. The sediment was air-dried, ground, and screened with a 2-mm sieve to remove large particles such as gravel and debris. The total organic carbon (TOC) and BC concentrations of the sediment were determined using a CHN elemental analyzer (Vario E1, Elementar Analysensyteme GmbH, Germany) as described in Liu et al.29 Sediment Spiking and Treatment. A certain amount of dry sediment was added to a series of 500-mL polyethylene beakers, followed by addition of dry MWCNTs, chars, or ash at mass ratios of 0, 0.2, 0.4, 0.6, 1.0, and 1.5%, respectively, making the mass of sediment and CMs to be 200 g in total in each beaker. Each amended system was physically mixed with a steel blender at 60 rpm for 24 h in the dark at room temperature. The sediment was then spiked with 1 mL of PFC methanol solution (20 mg L−1) and thoroughly mixed, making the sediment containing all of the PFCs together at a concentration of 0.1 mg kg−1 (100 ng g−1) for each PFC. Each amended system was placed in a fume hood for 3 h to evaporate methanol and thoroughly mixed again. Afterward, 300 mL of distilled water was added to make the mass ratio of water to sediment to be 1.5:1, mimicking real sediment−water systems, and the concentration in the aqueous phase was calculated to be ng L−1 level when the sediment was amended with two kinds of MWCNTs. The beakers containing sediment and water were then sealed, kept in the dark at 25 °C, and aged for 60 d. Each treatment consisted of three replicates.

BC on the bioaccumulation of PFCs in sediments, which will also provide information for the selection of potential remediation materials for soils and sediments contaminated with PFCs. Although PFC molecules have hydrophilic groups and hydrophobic and oleophobic C−F chains and they are different from other HOCs such as PAHs and PCBs, some research has suggested that hydrophobic interaction, rather than electrostatic attraction, dominates the sorption of PFOS on CMs.9,21,22 Therefore we hypothesize in this work that, similar to other HOCs, origin and concentration of CMs in sediments will affect the bioaccumulation of PFCs in benthic organisms, and the effects of CMs will differ in PFCs with different carbon chain lengths. Due to physiological tolerance to a range of environmental conditions, their residence in sediments, and ease of laboratory culture, Chironomus spp. are commonly used to evaluate the bioaccumulation of organic pollutants in sediments and associated sediment toxicity.17,23,24 The test organism used in this study is Chironomus plumosus larvae; it belongs to the family Chironomidae that consists of several thousand species with a worldwide distribution.25 The main objective of this study was to evaluate the effects of carbon nanotubes, chars, and ash on the bioaccumulation of PFCs with different carbon chain lengths by filter-feeding C. plumosus larvae in sediment. The PFCs included perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA), perfluorononanoic acid (PFNA), perfluorodecanoic acid (PFDA), perfluoroundecanoic acid (PFUnA), and perfluorododecanoic acid (PFDoA) which are prevalent in the environment. The sediment was amended with two multiwalled carbon nanotubes (MWCNTs), maize straw- and willowderived chars, and maize straw-origin ash; PFCs were spiked into the sediment and aged for 60 d. Larval body burden and aqueous phase concentrations of PFCs were measured after the bioaccumulation experiments. Uptake and elimination rate constants as well as biota accumulation factors were calculated; the effect of CM concentration and type on PFC bioaccumulation was compared, and the influence mechanism of CMs on PFC bioaccumulation was analyzed.

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MATERIALS AND METHODS Materials. PFOS (98%) was purchased from Tokyo Chemical Industries (Tokyo, Japan); PFOA (96%), PFNA (97%), PFDA (98%), PFUnA (95%), and PFDoA (95%) were obtained from Acros Organics (Morris Plains, NJ, USA). The physicochemical parameters of the PFCs are listed in Table S1 (Supporting Information (SI)). [1,2,3,4-13C4] perfluorooctane sulfonate (MPFOS) (≥99%) and [1,2,3,4-13C4] perfluorooctanoic acid (MPFOA) (≥99%) were supplied by Wellington Laboratories (Guelph, Ontario, Canada). Tetrabutyl-ammo12468

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Bioaccumulation Test. According to our previous study,15 C. plumosus larvae collected from the uncontaminated upper reaches of Yangliuqing River in the outer suburbs of Tianjin city were used for the PFC bioaccumulation experiments; PFCs in the larvae could not be detected. The organisms were acclimated to laboratory conditions in activated carbon-filtered tap water for 2 d, which served to purge their guts. Male larvae in third or fourth instars were selected for bioaccumulation experiments based on uniformity in size. At the end of the aging process of the sediment−water system, a total of 20 C. plumosus larvae (wet weight 350−450 mg collectively) were placed in each beaker. Each beaker was capped with a layer of gauze, and neither aeration nor food was provided to the larvae.15 All bioaccumulation experiments were conducted with a 16:8 (light:dark) photoperiod at 25 °C. Ranges of water quality parameters in the overlying water were temperature 25 ± 1 °C, DO 5.5−5.7 mg/L, and pH 7.6−7.7. For the kinetic experiments of PFC bioaccumulation, the duration time was set at 0, 1, 2, 3, 5, 7, 9, 11 d, respectively, for exposure; for the nonkinetic experiments, the duration time was set at 10 d for exposure. Larvae were removed from the sediment by sieving after the bioaccumulation experiments; the surviving larvae were counted, carefully washed, and allowed to depurate in distilled water for 6 h to empty their digestive tracts.15 The larvae were then freeze-dried for 48 h and ground into a fine powder for PFC extraction, which was conducted according to the ion-pairing method described by Kannan et al.30 Extraction procedure is shown in the SI. PFC concentrations in the larvae were reported on a dry weight basis; this was approximately five times higher than on a wet weight basis. Each experimental set was conducted in triplicate, and blank controls were set up with neither CMs nor PFC addition (n = 3). The lipid levels of C. plumosus larvae, determined using protocols described by Millward et al.,31 were 6.9 ± 0.4% on a dry weight basis before exposure, and did not change significantly after exposure according to our preliminary bioaccumulation experiments. PFOS Sorption on Sediment. To analyze the influence mechanism of CMs on PFC bioaccumulation in sediments, the sorption of PFCs on the CMs and sediment was studied and PFOS was selected as the representative PFC for sorption experiments. Because the sorption of PFOS on the CMs has been studied in our previous work,22 only the sorption of PFOS on the original sediment was studied in the present research, and the detailed procedure of the sorption experiment is shown in the SI. Aqueous Phase Measurement of PFCs in Bioaccumulation Test. Because the sorption of PFCs on pristine CMs might be different from that on CMs spiked in sediment, it might not be appropriate to predict PFC concentrations in aqueous phase of the sediment−water systems amended with CMs by using their sorption isotherms on pristine CMs. Therefore, W400 was selected as the representative CM for aqueous phase measurement of PFCs in the bioaccumulation test. Briefly, the test was conducted simultaneously as the same mentioned above, with the W400 concentrations of 0, 0.2, 0.4, 0.6, 1.0, and 1.5%, respectively, in sediments. After 10 d exposure, the water was decanted and centrifuged at 1431g for 15 min; the supernatant was sampled for PFC analysis. In the meantime, the larvae were removed from the sediment for PFC analysis. PFC Analysis. PFCs were analyzed using liquid chromatography−tandem mass spectrometry (LC-MS/MS; Dionex Ultimate 3000 and Applied Biosystems API 3200) in

electrospray negative ionization mode. A 10-μL aliquot of sample was injected into a 4.6 × 150 mm Acclaim 120 C18 column with 50 mM ammonium acetate and methanol as mobile phase. At a flow rate of 1 mL min−1, the mobile phase gradient was ramped from 70% to 95% methanol in 4 min, held at 95% methanol for 3 min, and then ramped down to 70% methanol in 3 min. The LC/MS/MS transitions used to monitor and quantify the analytes are listed in Table S1. Each sample was analyzed in triplicate. Concentrations of all target analytes were quantified from calibration curves drawn using external standards. The coefficient of determination for each calibration curve (7 point calibration, 0−200 μg L−1) was >0.99. The detailed procedure for quality assurance and quality control is shown in the SI. Data Analysis. All statistical analyses were performed using SPSS 13.0 (SPSS Inc., Chicago, IL, USA). Analysis of the variance (ANOVA, one factor) was carried out to test differences between each two compared groups. Difference was considered significant when the significance level was smaller than 0.05. The Pearson correlation coefficient was calculated and used to test the significance of correlation between each two variables.

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RESULTS AND DISCUSSION QA/QC Results. All procedural blank areas were less than half the determined limit of quantitation (LOQ) (S/N = 10) for each analyte with LC-MS/MS. Recoveries of the target analytes from the larvae tissue were between 87% and 96%, and the recoveries of MPFOS and MPFOA, mass spectrometric isotope spiked to the larvae samples, were between 91% and 100% (Table S1). All data were corrected according to the recovery indicators. Recoveries of PFCs were between 73% and 108% from the freshly spiked sediment and the sediment after aging and bioaccumulation (Figure S1), suggesting that little degradation or depletion occurred during the process of aging or bioaccumulation experiments. MWCNT10 amended (1.5%) sediment showed the lowest recoveries of the six PFCs; this was probably due to the fact that the strong sorption of PFCs by MWCNT10 would reduce the extraction efficiency. In addition, each PFC accumulated in the organisms was less than 1% of the whole spiked content in sediments, indicating that the bioaccumulation experiments did not break the equilibrium of PFCs among the sediment, CMs, and water. Characteristics of the Sediment and Carbonaceous Materials. The TOC in the original sediment was 2.18 ± 0.37%, and BC was 0.23 ± 0.03%. As shown in Table 1, W400 and M400 had C contents of 73.1% and 66.6%, respectively. The respective BET surface area of W400 and M400 was comparable to that (less than 10 m2 g−1) reported by Brwon et al.,32 but much lower than the reported values of 116 m2 g−1 by Chun et al.33 and 340 m2 g−1 by Braida et al.27 The different BET surface areas of laboratory-produced chars may be attributed to the diverse characteristics of the raw material and the different temperature for charring. Because MA was made in air, it had a lower C content than those of W400 and M400, but had a higher BET surface area. The BET surface area of MWCNT10 was approximately 1 order of magnitude higher than those of chars and ash. Bioaccumulation Kinetics and Biota−Sediment Accumulation Factors of PFCs. The survival rate of C. plumosus larvae was 92 ± 6.7% in the sediment−water system after bioaccumulation experiments; this indicates that there was no significant toxicity caused by the metal or ammonium in the 12469

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Table 2. Uptake Kinetic Parameters and Biota−Sediment Accumulation Factors of PFCs to C. plumosus Larvae in Sediments with Addition of 1.5% CMs (Average, Standard Deviation, n = 3, and the Individual 95% Intervals Were Not Wider than the Standard Deviation) without CMs

MA

M400

W400

MWCNT10

MWCNT50

chemical

ks (goc gdw−1 d−1)

ke (d−1)

r2

−1 BSAFdw kinetic (goc gdw )

−1 BSAFdw SS (goc gdw )

BSAF decrease rate (%)

PFOS PFOA PFNA PFDA PFUnA PFDoA PFOS PFOA PFNA PFDA PFUnA PFDoA PFOS PFOA PFNA PFDA PFUnA PFDoA PFOS PFOA PFNA PFDA PFUnA PFDoA PFOS PFOA PFNA PFDA PFUnA PFDoA PFOS PFOA PFNA PFDA PFUnA PFDoA

0.374(0.062) 0.120(0.032) 0.138(0.021) 0.158(0.009) 0.118(0.021) 0.128(0.012) 0.159(0.031) 0.043(0.010) 0.057(0.009) 0.046(0.012) 0.040(0.009) 0.048(0.012) 0.210(0.032) 0.069(0.012) 0.072(0.023) 0.070(0.023) 0.066(0.013) 0.066(0.020) 0.206(0.041) 0.063(0.013) 0.078(0.021) 0.077(0.013) 0.076(0.020) 0.069(0.012) 0.049(0.009) 0.029(0.009) 0.029(0.003) 0.006(0.002) 0.003(0.001) 0.002(0.000) 0.098(0.030) 0.046(0.010) 0.044(0.010) 0.018(0.003) 0.012(0.001) 0.013(0.003)

0.990(0.190) 1.104(0.211) 0.753(0.121) 0.986(0.192) 0.916(0.129) 0.900(0.092) 0.938(0.082) 0.818(0.093) 0.848(0.081) 0.765(0.093) 0.751(0.054) 0.753(0.090) 0.824(0.093) 0.891(0.023) 0.711(0.134) 0.654(0.120) 0.648(0.141) 0.609(0.060) 0.737(0.080) 0.705(0.200) 0.729(0.210) 0.728(0.130) 0.658(0.191) 0.592(0.120) 0.613(0.060) 0.862(0.020) 0.688(0.063) 0.613(0.063) 0.645(0.033) 0.518(0.010) 0.830(0.122) 0.990(0.134) 0.763(0.092) 0.377(0.034) 0.487(0.034) 0.579(0.023)

0.916 0.897 0.959 0.949 0.947 0.954 0.904 0.915 0.945 0.948 0.988 0.993 0.972 0.939 0.931 0.936 0.978 0.977 0.951 0.981 0.981 0.978 0.951 0.967 0.963 0.901 0.956 0.951 0.982 0.931 0.974 0.911 0.963 0.988 0.872 0.959

0.378(0.060) 0.108(0.022) 0.183(0.037) 0.160(0.032) 0.129(0.031) 0.141(0.021) 0.169(0.012) 0.053(0.013) 0.067(0.009) 0.061(0.013) 0.054(0.013) 0.059(0.003) 0.255(0.023) 0.077(0.013) 0.101(0.033) 0.106(0.013) 0.102(0.011) 0.109(0.020) 0.280(0.012) 0.089(0.013) 0.107(0.028) 0.107(0.010) 0.109(0.010) 0.117(0.021) 0.080(0.009) 0.037(0.003) 0.042(0.003) 0.010(0.002) 0.005(0.001) 0.004(0.0003) 0.118(0.034) 0.046(0.009) 0.058(0.009) 0.049(0.013) 0.025(0.009) 0.023(0.003)

0.394(0.024) 0.103(0.009) 0.169(0.012) 0.156(0.020) 0.142(0.019) 0.152(0.026) 0.174(0.012) 0.050(0.007) 0.067(0.012) 0.062(0.012) 0.055(0.008) 0.060(0.004) 0.259(0.029) 0.073(0.006) 0.100(0.012) 0.108(0.015) 0.103(0.014) 0.107(0.012) 0.283(0.030) 0.089(0.007) 0.109(0.014) 0.107(0.015) 0.112(0.014) 0.120(0.016) 0.080(0.007) 0.031(0.002) 0.042(0.003) 0.010(0.002) 0.005(0.0004) 0.004(0.001) 0.120(0.008) 0.044(0.004) 0.058(0.003) 0.048(0.004) 0.026(0.002) 0.022(0.005)

55 51 63 62 58 58 33 29 45 34 21 23 26 18 42 33 16 17 79 66 77 94 96 97 69 57 68 69 81 84

uptake rate constant of PFCs from the sediment (goc gdw−1 d−1), ke is the elimination rate constant (d−1), and t is the exposure time (d). Each PFC accumulated in the larvae was less than 1% of the whole spiked content in the sediment; those in the aqueous phase accounted for less than 5% of the total amount of PFCs in the sediment−water systems for most cases, except that PFOA, PFNA, and PFOS in the aqueous phase reached a maximum of 15% of the total amount when without CMs in sediment. Consequently, the nominal concentration of spiked PFCs in the sediment (0.1 mg kgsed−1, 4587 ng goc−1) could be regarded as Cs,oc to calculate the ks and ke values. As shown in Table 2, for the original sediment, the uptake rate constants ranged from 0.118 to 0.374 goc gdw−1 d−1, with PFOS having the highest value; the elimination rate constants ranged from 0.753 to 1.104 d−1, with PFNA having the lowest value. The uptake rate constants of PFCs in C. plumosus larvae obtained in this research were comparable to those in L. variegatus reported by Higgins et al.;20 while the elimination rate constants were higher than those in L. variegatus reported by Higgins et al.20 and in green mussels reported by Liu et al.35

sediments. No significant difference in survival rates could be observed among all bioaccumulation systems (p > 0.05). The average wet weight of individual larvae after the biaccumulation test did not change significantly when compared to the original mass added (p > 0.05). According to the uptake kinetic curves of PFCs (Figure S2), the time to reach steady-state for each PFC in larvae in different sediments was similar, suggesting that the time to reach steady-state condition was mainly controlled by the organisms themselves and the characteristic of each PFC. For example, only 3 d was needed for PFOA to reach the steady state, while PFDoA with the longest chain length reached steady-state at 5 d exposure. To determine the bioaccumulation kinetics, data from the uptake experiments were fit to the following first-order accumulation rate model:34 Ct =

Cs,ocks ke

(1 − e−ket )

(1)

where Ct is the concentration of PFCs in the larvae at time t (ng g−1 dry weight), Cs,oc is the organic carbon-normalized concentration of PFCs in the sediment (ng goc−1), ks is the 12470

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Figure 1. Body burden of PFCs in C. plumosus larvae in sediment with different types and concentrations of CMs.

This might be caused by the difference in physiological features of the test organisms. It was suggested that lipids were considered unlikely to be the biological reservoirs for PFCs,36 and very few data are reported for the lipid normalized biota−sediment accumulation factor (BSAF) for ionogenic organic contaminants such as PFCs. Therefore, nonlipid-normalized BSAF values of PFCs −1 (BSAFdw kinetic, ks/ke, goc gdw ) based on kinetic method were determined from the kinetic parameters, and the steady-state method was also used to calculate the BSAF values (BSAFdw SS , CB/Cs,OC, CB the concentrations of PFCs in the larvae at steady state).

As shown in Table 2, the BSAF values based on the kinetic method were very consistent with those based on the steadystate method. The result obtained in this research was different from the bioaccumulation result of PFCs in green mussels reported by Liu et al.,35 who found that the water-based bioaccumulation factors (BAF, CB/Cw, Cw the aqueous phase concentration of PFCs) obtained with the kinetic method were inconsistent with those obtained with the steady-state method. This was possibly due to the different organism and the different number of binding sites for PFCs in the organism; if the number of binding sites were much higher than the PFCs in organism, the bioaccumulation might also be viewed as a 12471

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partitioning process. The BSAFdw SS values of PFCs in the original sediment ranged from 0.10 to 0.39 goc gdw−1, lower than those in L. variegatus reported by Higgins et al.20 and Lasier et al.37 According to the measured concentrations of PFCs in the aqueous phase and larvae for the sediment−water system without CMs, the BAF value for each PFC was calculated. As shown in Figure S3, the BAF value increased with increasing carbon chain length. In addition, although the carbon chain length was identical for PFOA and PFOS, the BAF value of PFOS was approximately six times that of PFOA, suggesting that PFOS was much easier to bioaccumulate. Effects of CM Concentration on the Bioaccumulation of PFCs. Decreasing PFC bioaccumulation in C. plumosus larvae was found with increasing CM concentration in the sediment (Figure 1). For example, when the amended MWCNT10 concentration increased from 0 to 0.2, 0.4, 0.6, 1.0, and 1.5% in the sediment, the body burden of PFOS decreased from 1698 to 1337, 1104, 1006, 825, and 370 ng g−1 dry weight, respectively. The results obtained in this research were consistent with the previous results we obtained for the effect of black carbon amendments on PAH bioaccumulation by C. plumosus larvae,15 inferring that the effect of CMs on the bioaccumulation of PFCs in sediment was similar to that on PAHs. Further analysis showed that a linear positive correlation existed between the reciprocal of individual PFC concentration in larvae (CB, ng g−1) and CM concentration in sediment ( f CM, %) (p < 0.05) (Figure S4). To analyze the mechanism regarding the effects of CMs on PFC bioaccumulation, the sorption of PFOS, one of the most important PFCs, on the sediment amended with CMs was studied. As shown in Figure 2, although the sorption of PFOS on the original sediment fit

sediment, and the sorption of PFCs on original sediment might be different from that amended with CMs, a composite sorption model38 was used to describe the solid−water distribution of PFCs in the sediments amended with CMs: Q tot = fCM Kd,CMCw + fsediment Kd,sedimentCw

(2)

Equation 2 could be rewritten as the following: Kd,CM Kd,sediment 1 = fCM + f Cw Q tot Q tot sediment

(3)

where Cw is the aqueous phase concentration of each PFC (mg L−1); Qtot is the total sorbed concentration of each PFC in the solid phase including original sediment matrix and amended CMs (mg kgsolid−1); Kd,CM is the CM−water distribution coefficient of each PFC with the presence of sediment (L kgCM−1); Kd,sediment is the original sediment−water distribution coefficient of each PFC with the presence of CMs (L kgsed−1); and fsediment is the fraction of original sediment in solid phase. As mentioned above, PFCs in the aqueous phase accounted for less than 5% of the total amount of PFCs in the sediment− water systems for most cases and each of the sediments was spiked with the same quantity of PFCs, thus the nominal concentration of PFCs spiked in the sediment could be regarded as Qtot. In addition, fsediment only ranged from 98.5% to 100%. Therefore, for each PFC and CM, there should be a linear correlation between 1/Cw and f CM. As shown in Figure 3, the measured 1/Cw of each PFC did present a significant linear correlation with increasing W400 concentration in sediment (p < 0.01).

Figure 2. Sorption isotherm of PFOS on the original sediment (the sediment−water distribution coefficient kd = 10.7 L kg−1 when Ce less than 0.2 mg L−1).

Figure 3. Relationship between the reciprocal of measured PFC concentration in aqueous phase (Cw) and W400 concentration in the sediment.

the Langmuir model, the sorption was almost a linear distribution between the sediment and water when the sorption quantity was less than 10 mg kg−1. In addition, according to our previous research on sorption of PFOS on the five CMs studied here,22 the sorption was also a linear distribution between the CMs and water when the sorption quantity was less than 10 mg kg−1. As the nominal concentration of each PFC spiked in the sediment was 0.1 mg kg−1, the sorption of PFCs in the sediment amended with CMs probably was a linear distribution. Considering that the sorption of PFCs on pristine CMs might be different from that on CMs amended in

As shown in Figure S5, the body burden of PFOS in larvae was positively correlated with its aqueous phase concentration. Furthermore, as shown in Table S2, for each PFC, there was no significant difference in BAF values in systems with different concentrations of W400. This suggested that the bioaccumulation of PFCs was dependent on their freely dissolved concentrations in aqueous phase. That is to say, the freely dissolved PFC concentration in aqueous phase was an indicator of the potential for PFCs to partition into organisms in the sediments. The decrease of bioaccumulation with increasing 12472

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Table 3. CM−Water Distribution Coefficients of PFCs with the Presence of Sediment and the Sediment−Water Distribution Coefficients of PFCs with the Presence of CMs PFOS

PFOA

PFNA

CM−water distribution coefficients (Kd,CM, L kgCM−1) MWCNT10 1801 ± 90(5122a) 660 ± 33 MWCNT50 955 ± 95(2658a) 369 ± 18 MA 525 ± 26(1482a) 263 ± 16 M400 172 ± 26(1034a) 106 ± 7 W400 131 ± 7(993a) 75 ± 7 sediment−water distribution coefficients (Kd,sediment, L kgsed−1) MWCNT10 5.1 ± 0.3 (10.7b) 3.9 ± 0.2 MWCNT50 6.4 ± 0.6 4.6 ± 0.2 MA 7.7 ± 0.4 4.4 ± 0.3 M400 9.0 ± 1.3 4.6 ± 0.3 W400 7.7 ± 0.4 4.4 ± 0.4

PFDA

PFUnA

PFDoA

1209 677 572 248 93

± ± ± ± ±

60 34 28 12 9

2563 2289 1665 437 296

± ± ± ± ±

128 114 160 22 15

8764 6155 4166 938 517

± ± ± ± ±

438 307 208 140 51

15151 12835 7238 1199 1771

± ± ± ± ±

757 641 362 119 88

5.0 5.5 5.5 6.0 6.0

± ± ± ± ±

0.2 0.3 0.3 0.3 0.6

17.6 16.3 17.6 20.3 19.0

± ± ± ± ±

0.9 0.8 1.7 1.0 1.0

36.0 36.0 36.0 43.7 38.6

± ± ± ± ±

1.8 1.8 1.9 6.6 3.9

92.7 81.8 76.3 76.3 81.8

± ± ± ± ±

4.6 4.1 3.8 7.6 4.1

a

CM−water distribution coefficients of PFOS without the presence of sediment obtained from the results of our previous research.22 bSediment− water distribution coefficient of PFOS without the presence of CMs.

distribution coefficient of PFCs in the sediment which would result in a higher PFC concentration in the aqueous phase. The effect of CM amendment on the PFC bioaccumulation in sediment differed with the variation of PFC chain length. As shown in Table 2, for MWCNT10 and MWCNT50, the reduction of BSAF values increased with increasing PFC chain length except for PFOS; this is because CMs have a higher sorption affinity for PFC with a longer chain length, resulting in a lower aqueous phase concentration. Further analysis showed that the reduction rates of BSAF values were positively correlated with the Kow values (shown in Table S1) of the six PFCs (R = 0.9064, p < 0.05). Effects of CM Type on the Bioaccumulation of PFCs. The addition of identical concentration of carbon nanotubes, chars, and ash in the sediment resulted in different effects on PFC bioaccumulation; the BSAF values of each PFC differed with different CM amendments. MWCNT10/MWCNT50amended sediment reduced the PFC bioaccumulation in larvae to the greatest extent (Figure 1 and Figure S2). For example, compared to the nonamended sediment, addition of 1.5% chars, ash, and carbon nanotubes reduced BSAF values of PFCs by 16−45%, 51−63%, and 57−97%, respectively (Table 2). The reduction of PFC bioaccumulation by CMs followed the sequence of MWCNT10 > MWCNT50 > MA > M400 > W400. In addition, as shown in Table S4, the reduction rate of PFC bioaccumulation by the CM amendment in sediment was comparable to those of other HOCs such as PAHs and PCBs. The CM−water distribution coefficients (Kd,CM) of PFCs with the presence of sediment and the sediment−water distribution coefficient (Kd,sediment) of PFCs with the presence of CMs were obtained by plotting 1/CB against f CM based on eq 5. As shown in Table 3, for each PFC, the CM−water distribution coefficients (Kd,CM) followed the sequence of MWCNT10 > MWCNT50 > MA > M400 > W400, which was consistent with the sequence of BET surface area of the five types of CMs. Kd,CM values of PFOS with the presence of sediment were much lower compared to the pristine CMs. For example, the MWCNT10−water distribution coefficient of PFOS without the presence of sediment was approximately three times that with the presence of sediment. This was probably due to the fact that the surfaces of CMs would be seriously fouled by organic matter in the presence of sediment, thus reducing the effective surface. According to the results shown in Table 3, the sediment−water distribution coefficient

CM concentration was attributed to the reduction of the freely dissolved PFC concentrations in the aqueous phase caused by the sorption of PFCs on the CMs. Accordingly, the relationship between each PFC concentration in larvae (CB) and CM concentration (f CM) in sediment followed the equation CB =

BAF K d,CM

f

Q tot CM

+

K d,sediment Q tot

fsediment

(4)

where BAF is the water-based bioaccumulation factors of PFCs (L kg−1), and the meanings of the other parameters are the same as for eq 3. Equation 4 could be rewritten as the following: Kd,CM Kd,sediment 1 = fCM + f CB BAF·Q tot BAF ·Q tot sediment

(5)

This equation infers that 1/CB positively correlates with f CM, which is consistent with the results shown in Figure S4. In addition, fsedimentKd,sediment/(BAF·Qtot) in eq 5 should be almost identical for each individual PFC, while Kd,CM/(BAF·Qtot) should change with the variation of CM types and increase with the CM−water distribution coefficient. This agrees with the results shown in Table S3. Therefore, the present research suggests that both sorption and bioaccumulation of PFCs can be described by traditional linear partitioning under the studied conditions with low concentrations of PFCs. Although the BAF value of PFOS was lower than those of PFDA, PFUnA, and PFDoA (Figure S3), as shown in Table 2 and Figure S6, of the six PFCs, the body burden and BSAF values of PFOS were the highest regardless of the type and concentration of CMs added. This was probably caused by the higher aqueous phase concentration of PFOS in the sediment− water systems (Figure 3). Similarly, previous field studies showed that PFOS was much easier to accumulate in aquatic organisms compared to other PFCs.19,39 Compared to other HOCs, the BAF value of PFOS obtained in this research was much lower than those of phenanthrene (104.21), pyrene (105.11), and chrysene (105.67) in C. plumosus larvae in our previous work.15 However, the BSAFdw SS values of PFCs (0.103− 0.394) in the original sediment obtained in this research were much higher than those of phenanthrene (0.054), pyrene (0.044), and chrysene (0.014) by C. plumosus larvae in our previous work;17 this was probably caused by the lower 12473

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Notes

(Kd,sediment) of PFOS with the presence of CMs was little lower than that without the presence of CMs (10.7 L kg−1, Figure 3), suggesting that the presence of CMs might also exert influence on the sorption of PFOS on sediment. However, the sediment−water distribution coefficient for each PFC did not vary significantly with different types of CMs, suggesting that the effect of CM type was not significant. According to the results shown in Table 2, different types of CM amendment did not exert significant influences on the ke value of each PFC (p > 0.05). However, the uptake rate constant (ks) value of each PFC differed significantly with different types of CM amendment (p < 0.05), and followed the sequence of MWCNT10 < MWCNT50 < MA < M400 < W400 < without CMs. For instance, with a 1.5% amendment of these CMs, the ks values of PFOS decreased by 87%, 74%, 57%, 45%, and 44%, respectively, when compared to the sediment without CMs. This suggests that the uptake rate constant of PFCs was significantly influenced by the CM amendments, and the BSAF value was mainly affected by the uptake rate constant. This is due to the fact that the sorption of PFCs to carbonaceous materials will reduce their aqueous phase concentration and bioavailability. And as shown in Table 3, different types of CMs have different sorption affinities, leading to different ks values. For instance, the decrement of ks for PFOS was positively correlated with Kd,CM of the five types of CMs (R = 0.979, p < 0.01); MWCNT10 with the highest Kd,CM for PFOS resulted in the lowest ks value among the five types of CMs. In natural aquatic environments, larvae reside in sediment which provides organic matter as food for larvae. As PFCs will combine with organic matter, the ingestion of organic matter might be another route for PFC bioaccumulation in larvae. Furthermore, larvae might ingest CMs with associated PFCs, and this might affect the bioaccumulation of PFCs. Our previous research suggested that the MWCNT-associated PAHs may have been absorbed by larvae through particle ingestion.17 Therefore, in addition to PFCs in aqueous phase, further research is needed to study the effect of PFCs in the food (even in CMs) on their bioaccumulation in benthic organisms. If considering the CMs as potential remediation material for soil and sediment pollution with PFCs, ash might be an effective material. This is because the reduction of PFC bioaccumulation by ash was much higher than that by chars and little lower than that by MWCNTs (Figure 1), and the potential risks of CNTs are not well understood.40 In addition, ash is low cost and easy to obtain. For example, the annual production of maize straw exceeds 200 million tons in China, and a large proportion of it is field burned.

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The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This study was supported by the Major State Basic Research Development Program (2009CB421605 and 2010CB951104), National Science Foundation of China (51121003 and 51279010), and the Program for New Century Excellent Talents in University (NCET-09-0233). We thank Dr. Edwin Ongley for improving the English of the manuscript. We also thank the editors and anonymous reviewers for their constructive comments that improved this manuscript.

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ASSOCIATED CONTENT

S Supporting Information *

Additional information, including the physicochemical and analytical parameters of PFAs, comparison of experimental results on the effect of CMs on bioaccumulation of organic contaminants in sediment, and the relationship between the reciprocal of individual PFC concentration in larvae and CM concentrations in the sediment, etc. This material is available free of charge via the Internet at http://pubs.acs.org.

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REFERENCES

AUTHOR INFORMATION

Corresponding Author

*Phone: +86-10-58805314; fax: +86-10-58805314; e-mail: [email protected]. 12474

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