Accumulation and Elimination of Chromium by ... - Springer Link

Arch Environ Contam Toxicol (2008) 55:603–609 DOI 10.1007/s00244-008-9139-0

Accumulation and Elimination of Chromium by Freshwater Species Exposed to Spiked Sediments Mercedes Marchese Æ Ana M. Gagneten Æ Marıá J. Parma Æ Paola J. Pave´

Received: 24 August 2007 / Accepted: 21 January 2008 / Published online: 15 February 2008 Ó Springer Science+Business Media, LLC 2008

Abstract The bioaccumulation and elimination capacity of chromium were examined in four freshwater species: the submersed aquatic plant Ceratophyllum demersum (Ceratophyllaceae), the oligochaete Limnodrilus udekemianus (Tubificidae), the crab Zilchiopsis collastinensis (Decapoda), and the fish Cnesterodon decemmaculatus (Poeciliidae). All of the species were exposed simultaneously to sediments spiked with Cr (K2Cr2O7) at different concentrations for 28 days, followed by 7 days without Cr to evaluate the concentration of residual Cr. We found that Cr accumulated in the tissues of all four species. The highest bioconcentration factor obtained for each species is as follows: C. demersum, 718.66 (±272.91); L. udekemianus, 172.55 (±80.8), Z. collastinensis, 67.72 (±35.4); C. decemmaculatus, 23.11 (±12.82), all at 28 days of exposure.

Introduction Heavy metals are highly resistant to environmental degradation and can affect aquatic organisms as toxic substances in water and sediment, or as a toxicant in the food chain, with a strong tendency to bioaccumulate in aquatic life. There is a substantial literature on bioaccumulation, mainly of organic chemicals, in aquatic plants, oligochaetes, crabs,

M. Marchese M. J. Parma P. J. Pave´ Instituto Nacional de Limnologıá-INALI (CONICET-UNL), Jose´ Macia´ 1933, 3016, Santo Tome´, Santa Fe, Argentina M. Marchese (&) A. M. Gagneten M. J. Parma Facultad de Humanidades y Ciencias (FHUC-UNL), Ciudad Universitaria, 3000 Santa Fe, Argentina e-mail: [email protected]

clams and fishes (Ankley et al. 1992; Conrad et al. 2000; Egeler et al. 2004; van Hoof et al. 2001), but there is little information on chromium (Cr) accumulation in freshwater species (Dıás Correa et al. 2005; Ip et al. 2005; Nussey et al. 2000; Su et al. 2005; Van der Putte and Part 1982). Chromium is used in the production of steel and alloys, pigment manufacturing, plating, wood preservation, combustion of coal and oil, and leather tanning, which at higher concentrations causes serious environmental contamination in soil, sediments, and groundwater (Adriano 2001; Su et al. 2005). In natural waters two stable oxidation states of Cr persist (III and VI), which have contrasting toxicities, motilities, and bioavailability (Scott and Li 1996), and although at the cellular level Cr(III) might be toxic to organisms, Cr(VI) is the highest toxic form. This is highly soluble in water and a strong oxidizing agent that causes severe damage to cell membranes (Mei et al. 2002). Cr(III) is toxic because of its ability to form complexes with nucleic acids, proteins, and organic compounds (Su et al. 2005). Our objective was to evaluate the bioaccumulation potential and elimination of Cr by four freshwater species, enlarging the set of responses measured to characterize exposure and possible trophic transfer. Metal bioavailability, as measured by metal accumulation into the tissues of organisms, was also examined. The submersed aquatic plant Ceratophyllum demersum (Ceratophyllaceae), oligochaete Limnodrilus udekemianus (Tubificidae), crab Zilchiopsis collastinensis (Decapoda), and fish Cnesterodon decemmaculatus (Poeciliidae) were chosen for the present study because these species are representatives of the regional biota and colonize both lotic and lentic systems. They are also good candidates for use as sentinel organisms for their sedentary habits or scarce mobility and to belong at different trophic levels.

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The use of multispecies tests in the current study provides important information with ecological applications and it links toxicological effects at the individual and community levels (Landis and Yu 1999).

Materials and Methods In order to understand the complex ecological system, we reproduced a model with features that simulate the structure and function of natural systems using static mesocosms located outdoors (31°390 56.5100 S- 60°450 21.1900 W) during spring (September–October 2005) to investigate the responses of four species simultaneously. The tanks were covered with a net in order to avoid the input of allochthonous material. The water quality tested was similar to the hard water of the tributaries from the right margin of the Middle Parana´ River (Argentina). The study was conducted in six PVC tanks of 1000 L each, containing artificial sediment, composed of sand, kaolin clay, and peat (OECD 2004), and dechlorinated and aerated tap water. The Cr-spiked sediment was placed in each tank and overlying water was added to produce a sediment–water volume ratio of 1:4 (130 kg sediment and 800 L of water) and allowed to equilibrate for 5 days. Spiked sediments of the chosen concentration were prepared by the addition of a solution of the test substance directly to the sediment. A stock solution of the test substance dissolved in deionized water was mixed with the formulated sediment by hand mixing (OECD 2004). Macrophytes, oligochaetes, crabs, and fish were placed together in each tank and exposed to sediments spiked with Cr (K2Cr2O7) at nominal concentrations of 3 mg Cr(VI)/L (treatment 1, T1) and 6 mg Cr(VI)/L (treatment 2, T2), using two replicates per concentration, and a control (T0) under all the same conditions without the Cr. A preliminary experiment was conducted in order to optimize the test conditions of the definitive test [e.g., selection of test substance concentration(s), duration of the uptake, and depuration phases]. The 7-day elimination phase was governed by the period over which the concentration of Cr in the fish remains above the analytical detection limit. Ceratophyllum demersum and Z. collastinensis were collected in uncontaminated floodplain lakes; L. udekemianus were obtained from material commercially available as fish food. They were bred in the artificial sediment (OECD 2004) at 20 ± 2°C in ‘‘single-species’’ cultures and fed with a suspension of finely ground TetraMinÒ flakes. C. decemmaculatus were obtained from our own cultures. At the end of the stabilization period, 500 g of C. demersum, 200 g of L. udekemianus adults, 36

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specimens of Z. collastinensis, and 125 specimens of C. decemmaculatus (1.7–2.8 cm total length) were randomly distributed in each tank. Samples of water (1 L), sediment (250 g), macrophytes (10 g of leaves), oligochaetes (2–3 g), gills of crabs (two to three organisms), and fish (10 specimens pooled as a whole-body tissue) were taken in each tank to determine the total Cr concentration at 0, 1, 7, 14, and 28 days during the accumulation phase and at 1 and 7 days during the elimination phase. For this phase, the organisms were transferred to an aquarium with clean artificial sediment and dechlorinated tap water to evaluate the concentration of residual Cr. In both phases, a finely ground suspension of flaked fish food (TetraMin) was added every 2 days. The temperature and dissolved oxygen were measured daily with an oxymeter (YSI 55 model). The conductivity, pH, and salinity were checked daily with a Horiba U10 water meter; total hardness was checked by the titrimetric method (APHA 2005); ammonia and Cr(VI) concentrations were measured weekly by ultraviolet (UV)-visible spectroscopy. An aliquot of the sediment was taken from each tank at days 14 and 28 of the accumulation phase and centrifuged at 4500g for 30 min, after which the pore-water supernatant was carefully poured off for determination of Cr. For the determination of total Cr in water and pore water, samples were treated according to EPA Method 200.2 (US EPA 1991) and analyzed by atomic absorption spectrometry (Perkin-Elmer AAnalyst 800, with quantification limit of 3 lg/L and detection limit of 1 lg/L). For the determination of total Cr in sediment, samples were treated according to EPA Method 200.9 (US EPA 1991) and analyzed by atomic absorption spectrometry, with electrothermal atomization. Tissue samples were digested according to the EPA Method 200.3 (US EPA 1991) and analyzed by atomic absorption spectrometry. The oligochaetes were separated from the sediment and kept for 5–6 h in water for purging their gut contents and then the worms were rinsed to remove any remaining debris and were frozen. The crabs were washed with deionized water to remove adhering particles and the metal adsorbed onto the carapace, and they were frozen for 24 h before dissecting the gills of individuals with a plastic scalpel and forceps. The TOC (total organic carbon) concentration measured in the water column was obtained by the acidic sparging process. The procedure for AVS (acid-volatile sulfide) analysis followed the method described by Allen et al. (1993). Calibration curves, matrix spikes, apparatus blanks, and standard recoveries were employed in the analysis. Duplicate measurements showed that the concentrations of AVS were reproducible with an analytical precision better than 10%. A kinetic study was not performed to analyze the equilibrium concentrations of Cr in the organisms, but,


generally, for most contaminants, greater than 80% of a steady state between sediment and organisms is approached in 28 days of exposure (ASTM 1997; Ingersoll et al. 2003). Thus, the bioconcentration factor (BCF, tissue/water ratio) and the bioaccumulation factors (BAFs, tissue/sediment ratio) were calculated at the end of a 28-day exposure. The concept of BCF used in our study is the ratio of a chemical concentration in an organism to the concentration in water and BAFs is the ratio of a chemical concentration in an organism to the concentration in sediment. The BCF for the macrophytes, oligochaetes, crabs, and fish were calculated according to Newman and Unger (2003): BCF = (Ce – Ci)/Cw, where Ce = metal concentration in the tissue during Cr exposure [lg/g dry weight (dw)], Ci = the initial metal concentration in the tissue before Cr exposure (lg/g dw), and Cw = metal concentration in water (mg/L). The BAFs, the relation between the metal concentrations in the tissue and the sediment, was also calculated for L. udekemianus as follows: BAF = (Ce – Ci)/Cs, where: Ce = Cr concentration in tissue (lg/g dw) during Cr exposure, Ci = the initial Cr concentration in tissue (lg/g dw) before Cr exposure, and Cs = Cr concentration in sediment (lg/g dw). The BCF and BAFs were expressed as a function of the total weight of the macrophytes, worms, crabs, and fish samples. Normality of data or log-transformed data was checked using the Kolmogorov-Smirnov goodness-of-fit test. Analysis of variance (ANOVA) followed by the Tukey test was used to compare mean values (a = 0.05). When data or transformed data were not normally distributed (e.g., data of elimination phase), we used the nonparametric Kruskal-Wallis test followed by a multiple-comparison test to check for significant differences between treatments (a = 0.05).

Results The AVS concentrations in the sediment were always \1.0 mg/kg dw, and the TOC ranged from 4.52 to 7.58 mg/L (Table 1). No significant differences were registered in dissolved oxygen, temperature, conductivity, pH, salinity, and ammonia during the whole study period (ANOVA p [ 0.05). The ammonia concentration was relatively high due to the organisms excretion but was below the lethal concentration (21.4 mg/L) reported for benthic invertebrates by Schubauer-Berigan et al. (1995) and for nonsalmonid fish (0.5–4.6 mg/L (Rand and Petrocelli, 1985). Chromium concentrations in water and sediments among the control and the T1 and T2 tanks showed significant differences (p \ 0.001) and also between T1 and T2 (p \ 0.001) (Fig. 1). The Cr concentrations decreased

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in water and increased in sediment during the accumulation phase in T2. The Cr concentration in C. demersum, L. udekemianus, Z. collastinensis, and C. decemmaculatus (lg/g dw) increased rapidly, reaching the highest values between 7 and 14 days of exposure, showing that accumulation capacity is higher in the aquatic plant and oligochaete than in the crabs and fish (Fig. 2). It seems that the steady state is reached between 14 and 28 days by all of the species exposed in T2, whereas in T1, C. demersum and Z. collastinensis might not have attained equilibrium after 28 days of exposure. The concentrations of Cr in the tissues of the macrophytes, oligochaetes, crabs, and fish revealed significant differences (p \ 0.05) between the control and the treatments in the accumulation phase. On the other hand, the Tukey test only showed significant differences between the control and T2 (p \ 0.05) in the macrophytes, oligochaetes, and fish and between both treatments (p \ 0.05) in crabs. The weight of the crabs was not related to Cr concentration (r = –0.025). On the other hand, there were no significant differences in Cr concentration between female and male tissues (p [ 0.05). The Kruskal-Wallis test showed that there were no significant differences in concentrations between the control and treatments during the elimination phase (p [ 0.05). During the elimination phase, the Cr concentration in all of the species decreased immediately following the end of the exposure period only in T1, but it then increased at the end of this phase, except in L. udekemianus. On the other hand, the Cr concentration decreased in the tissue of aquatic plants and fish but not in crabs and worms at the end of elimination phase in T2 (Fig. 2). No dead organisms were recovered from either treatments or control units. An inverse relationship was observed between the BCF and the exposure concentrations in all species except C. demersum, where the plant tissue accumulation increased in the higher concentration of Cr (Fig. 3). The highest BCF obtained for C. demersum was 718.66 (± 272.91) in T2; for L. udekemianus, it was 172.55 ( ± 80.8); for Z. collastinensis, it was 67.72 (± 35.4); and for C. decemmaculatus, it was 23.11 (± 12.82) in T1 at 28 days. The BAFs obtained in oligochaetes was higher at 14 days than at 28 days of exposure (Fig. 4).

Discussion Because of their widespread release and persistent nature, concentrations of metals such as chromium, cadmium, copper, lead, nickel, silver, and zinc are commonly elevated in aquatic sediments. These metals, in addition to

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Table 1 Average values (± SD) of environmental variables measured in water (except AVS in sediment) during accumulation and elimination phase in all the treatments Accumulation phase T0 Oxygen (mg/L)

Elimination phase

T1

T2

T0

T1

T2

9.0 (± 0.96)

8.9 (± 0.78)

8.9 (± 0.84)

7.4 (± 0.05)

7.8 (± 0.44)

7.8 (± 0.53)

Temperature (°C)

17.8 (± 2.66)

17.5 (± 2.42)

17.6 (± 2.41)

21.4 (± 1.98)

21.4 (± 1.37)

21.6 (± 1.24)

Conductivity (lS/cm) pH

1294 (± 69) 8.29 (± 0.13)

1219 (± 45) 8.30 (± 0.12)

1233 (± 64) 8.30 (± 0.12)

1470 (± 70) 8.37 (± 0.05)

1470 (± 50) 8.43 (± 0.09)

1480 (± 62) 8.43 (± 0.09)

Salinity (%)

0.05 (± 0.00)

0.05 (± 0.00)

0.05 (± 0.00)

0.07 (± 0.00)

0.07 (± 0.00)

0.07 (± 0.00)

Ammonia (mg/NH3–N)

0.65 (± 0.09)

1.34 (± 0.59)

1.43 (± 0.73)

0.47 (± 0.17)

0.42 (± 0.17)

0.57 (± 0.18)

Hardness (mg/L CaCo3)

320 (± 35.9)

295 (± 53.8)

290 (± 30.2)

281 (±5.76)

307 (± 51.9)

317 (± 38.2)

\1.0 (± 0.0)

AVS (mg/kg) TOC (mg/L)

\1.0 (± 0.0)

6.59 (± 0.81)

Water column Cr (VI) (mg/L) Pore water (Cr mg/L)

0.02 (± 0.01) 0.003 (± 0.0)

6.44 (± 0.70) 0.27 (± 0.16) 0.003 (± 0.0)

\1.0 (± 0.0) 5.80 (± 1.09) 0.90 (± 0.24) 0.006 (± 0.0)

nd

nd

nd

nd

nd

nd

0.04 (±0.00)

0.01 (± 0.00)

0.03 (± 0.01)

nd

nd

nd

nd: no determined. N = 42. T0: control, T1: treatment at 3 mg Cr (VI)/L, T2: treatment at 6 mg Cr (VI)/L

Chromiun concentration

100 Water (mg/l)

Sediment (µg/g dw)

10

1 0 1 7 14 28 (days) T0

0 1 7 14 28 0 1 7 14 28 T1 T2 Accumulation phase

1 7 1 7 1 7 T0 T1 T2 Elimination phase

Fig. 1 Mean and standard deviation of the mean of Cr concentrations in water and sediment in each treatment during accumulation and elimination phase. Bars represent +1 SD

nonionic organic chemicals in contaminated sediments, are a significant pollutant source that might cause water quality degradation to persist, even when other pollutant sources are stopped (Burgess and Scott 1992; Ingersoll et al. 1995; Salomons et al. 1987). The basic routes of exposure for organisms are transport of dissolved contaminants in pore water or water overlying across biological membranes and ingestion of contaminated food or sediment particles with subsequent transport across the gut. In this study, the high water hardness would make the Cr less bioavailable; however, at the end of the 28-day exposure period, all of the species had bioaccumulated Cr. The macrophytes, together with benthic invertebrates (oligochaetes and crabs), showed the highest capacity of accumulating Cr, in concentrations 50–700 times higher than those found in water and participating, in this way, in pollutant dynamics. On the other hand, the fish showed a lower BCF (23) but higher than the BCF (\3) reported for rainbow trout by Calamari et al. (1982). Courdassier et al. (2005) reported for other aquatic species

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(e.g., for snails) exposed to Cr a BCF of 50.8. These results differ from the findings of other workers who reported that Cr did not concentrate strongly in specific tissue (Luoma and Rainbow 2005; Pourang et al. 2004). However, the variability in metal bioaccumulation among species is common and Luoma and Rainbow (2005) reported that concentrations in the tissue of different animal species varied by seven orders of magnitude. Moreover, interpretation of bioaccumulation data is complicated by the presence of both absorbed and adsorbed forms of metals, with the adsorbed form not incorporated into tissue but contributing to the overall body concentration. The L. udekemianus BAFs from sediment appear notably lower than the corresponding BCF. This demonstrates, as reported by Egeler et al. (1999), that the extrapolation of the BCF to other environmental compartments such as sediment is not possible. On the other hand, the BAF differs from a BCF in that the chemical concentration in the aquatic organism results from all possible routes of exposure (dietary absorption, transport across the respiratory surface, etc.) (Gobas and Morrison 2000). The higher tissue concentrations were obtained in organisms exposed to lower concentrations, so there is probably a threshold value for different invertebrates and fish, above which Cr incorporation is not proportional to the exposure concentration. Similar trends was reported by McGeer et al. (2003) and DeForest et al. (2007), who observed for a variety of aquatic organisms an inverse relationship between BCF and exposure concentration. However, the plants showed a rapid uptake of Cr at higher concentrations, which might be related to Cr toxicity where, through broken cell membranes, plants might have passive uptake of a large amount of the metal, as reported by Vazquez et al. (1987) and Maine et al. (2004).


607

10

6 T0

T1

ug Cr/g dw

5

T2

BAFs

4 3 2 1 0

1

7

14

28

1

7

1

Days exposure

0 14

100

ug Cr/g dw

T1

Fig. 4 Bioaccumulation factor (tissue/sediment) of L. udekemianus at 14- and 28-day Cr exposure in both treatments. Bars represent +1 SD

10

1 1

7

14

28

1

7

1

7

Days exposure 100

T2

ug Cr/g dw

28 Days exposure

10

1 1

7

14

28

Days exposure

C.decemmaculatus

Z. collastinensis

L. udekemianus

C.demersum

Fig. 2 Chromiun concentrations in each freshwater species during the accumulation and elimination phases. T0: control, T1: treatment 1 (3 mg Cr/L); T2: treatment 2 (6 mg Cr/L). The values were transformed in x + 1

1000

T1 T2

BCF

100

10

1 C. demersum

L. udekemianus

Z.collastinensis

C. decemmaculatus

Fig. 3 Bioconcentration factor (tissue/water ratio) at 28-day Cr exposure in both treatments. Bars represent +1 SD. T1: treatment 1 (3 mg Cr/L); T2: treatment 2 (6 mg Cr/L)

Many factors influence the elimination of metal from the tissues, such as temperature, pH, hardness water, age, metabolic activity, and the biological half- life of the metal (Heath 1987; Holdway 1988; Larsson et al. 1985). In our study, a rapid tendency to elimination of the accumulated Cr was observed when the organisms were transferred to clean water; however, the 7-day elimination phase was not enough for the tissue depuration in all the species analyzed. Passive elimination might occur across the gills, kidneys, and integument, and although there are differences in detoxification systems among species, the detoxification route depends on the physicochemical properties of the metal. Freshwater fish can excrete a higher than normal proportion of their metal intake under contaminated conditions and thus maintain trace metal concentrations in the body at a normal level (Leland and Kuwabara 1985). On the other hand, Heath (1987) reported that fish can excrete metals, and under continuous exposure to a water-borne chemical, the excretory processes might take several hours or days to become activated. Thus, the body burden can rise rapidly and then actually decline somewhat with continued constant exposure. The AVSs can react with cationic metals to make insoluble metal sulfides and can thereby control pore-water metal concentrations (Lee et al. 2000). In this study, the AVS was \1 mg/kg and the pore-water Cr concentrations were low (Table 1), although the Cr was available from the environmental media for accumulation into benthic organisms according to the BCF and BAFs obtained. Many dissolved metals readily bind to dissolved (actually colloidal) organic carbon (DOC), forming complexes that do not appear to be bioavailable (Bergman and Dorward-King 1997) and metals associated with organic matter might become available through the digestive process (Meyer et al. 2005). However, Honeycutt et al. (1995) have shown that metals can be stored mainly in the digestive tracts and in the body walls of oligochaetes. In

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Limnodrilus hoffmeisteri, metals are stored in rich sulfur granules in particular cells called chloragocytes, which form the chloragogen tissue covering the digestive tract (Klerks and Bartholomew 1991; Klerks and Levinton 1989). Another method of detoxification occurs in oligochaetes of the genus Tubifex, where the metals are stored in the caudal part of the worm, which is eventually lost (Lucan-Bouche´ et al. 1999). The submersed aquatic plants C. demersum can act as powerful agents of Cr removal from the environment, as demonstrated in this study. On the other hand, Maine et al. (2004) reported that floating macrophytes such as Salvinia herzogii and Pistia stratiotes have the ability to absorb Cr specifically in the roots and can withstand high concentrations of this metal. In general, aquatic macrophytes can have beneficial effects by purifying nutrients and detoxifying toxic substances (Behrends et al. 1994; Hammer and Bastian 1989). In Z. collastinensis, Cr increased in gills during the detoxification phase, showing that they take part in the elimination. Investigations of the pattern of Cr distribution in the gills of crabs and mantle and gills of mollusks indicate that Cr is deposited and immobilized at the external surface (Dias Correa et al. 2005; Saha et al. 2005). These organs are responsible for transferring Cr toward the organism and take part in metal detoxification. The mechanism involved, which was proposed by Dias Correa et al. (2005), is that the gills are the first site in which Cr aggregates are formed with organic molecules of glutathione, ascorbic acid, and saccharides, forming organometallic complexes. The crustaceans also concentrate metals in their exoskeleton and eliminate metals via a normal physiological phenomenon: moulting; similarly, worms use an amputation process to adapt to contaminated media (LucanBouche´ et al. 1999; Ravera 2001). Zilchiopsis collastinensis is occasionally consumed by humans, so it could also act in the trophic transfer of Cr to humans. Metals in invertebrate tissues also represent a concentrated source that might be toxic in the diet of fish (Woodward et al. 1994). Farag et al. (1999) concluded that ingestion of metal-contaminated invertebrates might be the principal route of metal exposure to fish. We can conclude that all of the taxa tested in this study accumulate Cr and might therefore be proposed as biomonitors of contamination of freshwater environments. The measurements of metal concentrations in the tissues of biomonitors reflect the bioavailability of the metal in the environment. However, C. demersum, L. udekemianus and Z. collastinensis are better biomonitors than C. decemmaculatus because of their higher capacity to accumulate Cr. The 7-day elimination phase was enough to obtain a significantly reduction of Cr by C. decemmaculatus but not for C. demersum, L. udekemianus, and Z. collastinensis.

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Arch Environ Contam Toxicol (2008) 55:603–609 Acknowledgments This survey was supported by grants from the Universidad Nacional del Litoral and Agencia para la Promocioń Cientı´fica y Tecnolo´gica, Argentina (Proyect PICTO No. 13224 UNL-ANPCyT). Chromium concentrations were determinated in Servicio Centralizado de Grandes Instrumentos (CERIDE-CONICET), Laboratory in the Proficiency Testing Program Canadian Association for Environmental Analytical Laboratories (CAEL). We also thank the International Science Editing for revising the English.

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