Cadmium and zinc interactions and their transfer in
Ž. The Science of the Total Environment 285 2002 187᎐ 195 Cadmium and zinc interactions and their transfer in soil-crop system under actual field conditions Zhongren Nan a,b, U , Jijun Li b , Jianming Zhang b , Guodong Cheng a a State Key Laboratory of Frozen Soil Engineering, Cold and Arid Regions En¨ironmental and Engineering Research Institute, CAS, Lanzhou 730000, PR China b Department of Geography, Lanzhou Uni¨ersity, Lanzhou 730000, PR China Received 17 December 2000; accepted 1 June 2001 Abstract The transfer of Cd and Zn from calcareous soils nearby a non-ferrous mining and smelting bases to the spring Ž.Ž. wheat Triticum aesti ¨um L. and corn Zea mays L. tissues and the interactions between the two metals concerned were investigated under actual field conditions. Samples of soils and entire crops were randomly collected during Ž harvest time in 1998 in the Baiyin region. The soil metal contents showed that the furrows had been polluted mean y 1 y1 . values: 3.16 mg kg for Cd; 146.78 mg kg for Zn and the significant spatial variation of the soil contamination Ž y 1 y1 . existed here ranges, Cd: 0.14᎐ 19.3 mg kg ; Zn: 43.5᎐ 565.0 mg kg . The translocation ratios of the two metals from soil to crop parts in the region studied were relatively lower and the order of the element transfer in different plant tissues was root) stem) grain. The transfer ratio of element Cd was lower than that of element Zn. Cd and Ž. Zn uptake by the crop structures could be best described by four models P- 0.01 : linear; exponential; quadratic; and cubic. Apart from a linear relationship between the element Cd in the corn grains and soils, models were generally non-linear. An analysis of Cd᎐Zn interaction mechanism led to the conclusion that the effects of the two metals were synergistic to each other under field conditions, in which increasing Cd and Zn contents in soils could increase the accumulations of Zn or Cd in the two crops. ᮊ 2002 Elsevier Science B.V. All rights reserved. Keywords: Cadmium; Zinc; Spring wheat; Corn; Transfer and interaction; Baiyin U Corresponding author. Ž. E-mail address: zhaochy@nwnu.edu.cn Z. Nan . 0048-9697r02r$ - see front matter ᮊ 2002 Elsevier Science B.V. All rights reserved. Ž. PII: S 0 0 4 8 - 9 6 9 7 01 00919-6 () Z. Nan et al.r The Science of the Total En ¨ironment 285 2002 187᎐ 195188 1. Introduction Toxic heavy metal contamination in soils and crop plants is of major importance due to their health effects on humans and other animals Ž. Farmer and Farmer, 2000; Pichtel et al., 2000 . Ž. Ž. Cadmium Cd is a toxic element and zinc Zn is toxic in high concentrations, and numerous inves- tigations showed that the pronounced amounts of Cd and Zn were often found in arable soils adja- cent to a non-ferrous metal production bases Ž Pierzynski and Schwab, 1993; Dudka et al., 1996; . Dahmani-Muller et al., 2000 . The processing and subsequent release of zinc to the environment is normally accompanied by cadmium environmen- Ž. tal pollution because of zinc ores ZnS generally containing 0.1᎐5% and sometimes even higher Ž. cadmium Adriano, 1986 . The trace elements concerned entered the soils mainly from sludge- borne heavy metal applications and industrial wastewater irrigation, and partially from aerial deposition and the usage of fertilizers and pesti- Ž cides Mench et al., 1994; Ullrich et al., 1999; Nan . and Zhao, 2000; Sterckeman et al., 2000 . Heavy metal uptake by roots depends on both Ž soil and crop plant factors e.g. source and chemi- cal form of elements in soil, pH, CEC, organic . material, plant species and tissues, plant age, etc. . Interactions among the co-exist elements occur- ring at root surface and within the plant also affect uptake and translocation. Cadmium, unessential to plants, and zinc, essential to plants, are elements having similar geochemical and en- vironmental properties. This association of cadmium and zinc in the environment and their chemical similarity can lead to interaction between cadmium and zinc during plant uptake, transport from roots to aboveground parts, or Ž. accumulation in edible parts Das et al., 1997 . Accumulation of heavy metals in crop tissues and transfer of them in soil crop system had well Ž been documented Dudka et al., 1996; Barman et . al., 2000; Kisku et al., 2000 . Interactions of Cd and Zn and their accumulation in plant parts in solution culture or in pot experiment had been Ž reported Coughtrey and Martin, 1979; Smilde et al., 1992; Moraghan, 1993; Mckenna et al., 1993; . Dudka et al., 1994; Zhou et al., 1994 . However, to our knowledge, there is little information about the fates and behaviors of the metals in crop tissues in fields. Therefore, the present investiga- tion was undertaken to examine the interactions between cadmium and zinc in arable soils and their effects on the accumulation of both metals Ž in crop structures. Spring wheat Triticum aes- .Ž . ti ¨um L. and corn Zea mays L. were chosen because they are staples in the diet of the local people in the northern China, and both of the crops readily absorb Cd and Zn from Zn᎐Cd Ž contaminated soils Hinsely et al., 1984; Dudka et . al., 1994 . The goals of our study were to examine Ž. in these two crops: 1 distribution patterns of cadmium and zinc contents in different parts of the two crops grown in the field influenced by non-ferrous metal mining and smelting operation; Ž. 2 transfer ratios and relationship models of the two metals concerned from soils to plant parts; Ž. and 3 effects of Cd᎐Zn interactions on the concentrations of both metals in crop tissues. 2. Materials and methods The work was carried out in the Baiyin region, where, 36Њ23Ј to 36Њ40Ј N, latitude and 104Њ to 104Њ25Ј E, longitude, one major non-ferrous met- als mining and smelting base in China was built in the 1950s. The region studied is geographically located in calcareous soil zone in the northern China with a surface area of approximately 501 km 2 divided into two basins by the watershed, i.e. Dongdagou stream basin and Xidagou stream basin, both of which accept treated or untreated domestic wastewater and industrial sewage. The soil parent material was Chinese loess and the Ž. soil texture was loam, clay content - 0.01 mm 35.18%. Soil pH ranged from 7.35 to 9.31, mean value 8.66" 0.4. The organic matter content was low, mean value 1.45" 0.59% and the content of Ž. available phosphorous P O varied widely from 25 6.4 to 287.7 mg kg y1 DW in the cultivated soil studied. The soils in this region are considered impor- tant croplands because most cereals for the local people are produced there. Due to the shortage of irrigated water and under the direction of the () Z. Nan et al.r The Science of the Total En ¨ironment 285 2002 187᎐ 195 189 wastewater land treated policy, this region has a long history of using the industrial and domestic wastewater to irrigate or partially irrigate furrows. The contents of soil metals concerned, particu- larly of soil Cd, had shown a considerable amount Ž. of pollution Nan and Zhao, 2000 . The sampling region consisted of three areas according to the types of irrigation water, i.e. one Ž. area irrigated with Yellow River water YA , one with the mixture of wastewater and Yellow River Ž. Ž. water MA and one with wastewater WA . Soil and entire crop samples were randomly collected during harvest time in 1998 throughout the three areas. Soil samples were vertically obtained with a depth of 0 to 20 cm from each crop root zone. Entire crops were obtained by way of digging and the roots were washed in place and again back at laboratory to clean further. The crop was separated into roots, stems and grains. The specimens were washed with tap wa- ter and distilled water followed by demineralized water. Special attention was given to the roots, which were scrubbed free of soil and rinsed thoroughly. All crop samples were stored in the brown paper bags, dried in an oven at 70ЊC for 12 h, and then ground in a stainless steel mill for metal analysis. All soil samples were air-dried at room temperatures and purified by passing through a 1-mm sieve in order to eliminate foreign matters. Fractions less than 1 mm were ground further in an agate mortar. Homogenized samples were sealed in polyethylene bags for analysis. Ž. Two grams of crop root, stem and grain sam- ple was dissolved in the mixture of HO᎐ HClO ᎐ HNO , and 0.5 g of air-dried 22 4 3 soil sample in the mixture of HCl᎐ HNO ᎐ HClO ᎐HF. These samples were digested 34 Ž. in a Taflon-PFA using MDS-9000 ORIENT . The concentrations of selected heavy metals were de- Ž. termined by ICP Rodushkin et al., 1999 . For all analyses, control standard solutions were run at the start, during and at the end of sample runs to ensure continued accuracy. Analytical precision of the method was improved by including several Ž. duplicate samples 10% of total . Reproducibility was within "5%. Data were analyzed using one-way ANOVA Ž. LSD and curve estimation. All statistical analy- ses were done through using the statistical pack- age SPSS10.0 and Excel’97 for Windows. 3. Results Contents of Cd and Zn in soils and results of one-way ANOVA are given in Table 1. Soil cadmium content at WA was significantly differ- ent from others by LSD at P- 0.05 but the findings of one-way ANOVA showed that the soil metal contents did not significantly differ between YA and MA. The values of soil zinc significantly differed across areas studied by LSD at the 0.05 probability level. Table 2 shows the concentrations of the metals concerned in crop structures and the results of one-way ANOVA. The accumulation ratios of heavy metal concentration between crop parts and soil and their proportions are listed in Table 3. It can be seen that the metal contents in two crop parts from YA and MA did not differ much but the levels of these metals in the tissues of two plants from WA was significantly different from those from others by LSD at P- 0.05. Trace elements concerned were markedly different Table 1 y1 Ž. Contents of Cd and Zn in the soils in different areas mg kg DW, "S.D. Area Spring wheat lands Corn lands N Cd Zn N Cd Zn U U YA 16 0.22" 0.05 59.16" 9.33 13 0.22" 0.06 60.09" 9.74 U U MA 18 0.59" 0.28 160.95" 129.58 11 0.50" 0.21 95.01" 19.68 UU UU WA 13 10.36" 4.42 235.01" 73.48 9 10.11" 3.46 227.35" 67.33 Nssample size. Detection limits: - 0.01 ppm for Cd, - 0.005 ppm for Zn. An asterisk indicates this area has significant difference with others by LSD at P- 0.05. () Z. Nan et al.r The Science of the Total En ¨ironment 285 2002 187᎐ 195190 Table 2 y1 Ž. Concentration of Cd and Zn in the crop tissues in different areas mg kg DW, "S.D. Area Spring wheat Corn N Cd Zn N Cd Zn Grain 16 0.05" 0.03 25.38" 6.27 13 0.05"0.03 16.02" 3.74 YA Stem 16 0.07" 0.02 35.69" 5.44 13 0.16"0.07 18.35" 3.77 Root 16 0.23"0.16 35.56" 8.42 13 0.21" 0.11 43.71" 10.83 Grain 18 0.05" 0.04 31.08" 7.38 11 0.05"0.03 15.71" 3.66 MA Stem 18 0.11"0.07 33.31" 6.70 11 0.26" 0.11 21.28" 7.66 Root 18 0.50"0.27 33.94" 10.11 11 0.44" 0.20 61.40" 18.24 Grain 13 0.61" 0.41 42.03" 17.92 9 0.58"0.16 22.85" 3.21 U WA Stem 13 1.91" 1.32 83.01" 29.39 9 5.06"1.68 42.05" 18.97 Root 13 6.92"4.32 229.72" 104.68 9 8.42" 2.59 145.45" 46.28 Nssample size. Detection limits: - 0.01 ppm for Cd, - 0.005 ppm for Zn. An asterisk indicates this area has significant difference with others by LSD at P- 0.05. between roots, stems and grains. The two metals in the whole region were highest in roots, fol- Ž lowed by stems and then low in grains Figs. 1 and . 2. Curve estimation regression analysis was used to highlight the relationships between the trace metal concentrations in crop structures and in soils and their interactions. Trends in metal con- centrations in crop parts concerned as a function of trace metal contents in the soils studied were Ž. best described by relationship models Table 3 . Apart from a linear relationship between the element Cd in the corn grains and soils, models were generally non-linear. Table 4 summarized the regression models describing the Cd and Zn levels in crop tissues with the contents of the Ž. metals in soils. All correlation coefficients R Ž. were found to be significant P- 0.01 and posi- tive. These findings showed there existed the syn- ergistic effects of each other, in which increasing Table 3 Relationships between the trace metal concentrations in crop parts and in soils Parts Equation R d.f. P Ž. Spring wheat Triticum aesti ¨um L. 0.2067wCdsx wx Grain Cd s 0.0409e 0.79 35 0.000 2 y 63 wx wx wx wx Zn s2.5448q0.4911 Zns y 0.0019 Zns q 2= 10 Zns 0.48 43 0.01 0.2536wCdsx wx Stem Cd s0.082e 0.91 38 0.000 2 wx wx wx Zn s6.8026q0.4431 Zns y 0.0007 Zns 0.65 44 0.000 2 wx wx wx Root Cd s0.2275q0.3346 Cds q0.0255 Cds 0.97 43 0.000 2 wx w x w x Zn sy72.410q1.7650 Zns y0.0029 Zns 0.66 44 0.000 Ž. Corn Zea mays L. wx w x Grain Cd s 0.0383 q0.0526 Cds 0.99 29 0.000 2 wx wx wx Zn s8.0261q0.1351 Zns y 0.0003 Zns 0.60 30 0.001 2 wx w x w x Stem Cd s0.0090q0.5785 Cds y0.007 Cds 0.98 28 0.000 0.0044wZnsx wx Zn s13.7929e 0.77 31 0.000 23 wx wx wx wx Root Cd sy0.1122q1.2719 Cds y 0.058 Cds q 0.0019 Cds 0.99 28 0.000 2 wx w x w x Zn sy11.700q0.9604 Zns y0.0012 Zns 0.87 29 0.000 wx w x X denotes the content of x element in crop parts, and Xs in soils. () Z. Nan et al.r The Science of the Total En ¨ironment 285 2002 187᎐ 195 191 Fig. 1. Boxplots of cadmium concentrations in crop tissues from Baiyin region, averaged across three areas. Cd or Zn content in soils may increase Zn or Cd accumulation in crop plant tissues, respectively. 4. Discussion Soil contents in excess of 1 mg Cd kg y1 soil are considered to be evidence of anthropgenic pollu- Ž. tion Uminska, 1993 , and the background levels of the metals in Chinese gray calcareous soils were 0.072 and 55.1 mg kg y1 for Cd and Zn, Ž. respectively Wang and Wei, 1995 . Contents of the metals concerned in soils studied showed that the furrow had been contaminated compared with the background levels and the literatures. Contents of heavy metals studied in three areas Fig. 2. Boxplots of zinc concentrations in crop tissues from Baiyin region, averaged across three areas. showed markedly spatial variation. The highest contents in soils occurred at WA. Soil Cd concen- tration at WA was 47 and 17 times higher than the contents found at YA and MA in spring wheat lands, respectively, and 46 and 20 times in corn lands, respectively. Soil Zn concentration at WA was 4 and 1.5 times higher than the contents found at YA and MA in spring wheat lands, respectively, and 4 and 2.4 times in corn lands, respectively. These facts could be the result of differences mainly in irrigation water. The WA was the only one area adjacent to the non-ferrous smelters and could be irrigated with the mixture of industrial effluent and domestic wastewater. These findings confirmed irrigation with Yellow River water and the mixture of Yellow River water and domestic wastewater rather than with Table 4 Regression models between contents of trace metals in the crop parts and soil Cd and Zn levels Parts Equation R d.f. P Ž. Spring wheat Triticum aesti¨um L. 0.006wZnsx wx Grain Cd s 0.0343e 0.50 35 0.001 23 wx wx wx wx Zn s25.9183q6.4297 Cds y0.6550 Cds q0.0188 Cds 0.50 43 0.006 0.0063wZnsx wx Stem Cd s 0.0753e 0.50 38 0.001 23 wx wx wx wx Zn s28.5867q15.312 Cds y1.5869 Cds q 0.0565 Cds 0.87 43 0.000 2 wx w x w x Root Cd sy3.6281q0.0646 Zns y 0.0001 Zns 0.65 43 0.000 23 wx wx wx wx Zn s17.1219q43.742 Cds y2.5710 Cds q0.0498 Cds 0.88 43 0.000 Ž. Corn Zea mays L. wx w x Grain Cd sy1.4666q0.3623ln Zns 0.82 29 0.000 23 wx wx wx wx Zn s14.4638q4.3836 Cds y0.5641 Cds q0.0203 Cds 0.69 29 0.000 0.0168wZnsx wx Stem Cd s 0.0614e 0.86 29 0.000 23 wx wx wx wx Zn s18.1717q3.5387 Cds q0.1759 Cds y 0.0223 Cds 0.71 29 0.000 0.0174wZnsx wx Root Cd s 0.0839e 0.88 30 0.000 23 wx wx wx wx Zn s33.5841q54.697 Cds y6.6099 Cds q0.2214 Cds 0.89 28 0.000 wx w x X denotes the content of x element in crop parts, and Xs in soils. () Z. Nan et al.r The Science of the Total En ¨ironment 285 2002 187᎐ 195192 Table 5 Accumulation ratios of heavy metal concentration between crop parts and soil and their proportions Cd Zn GrSStrSRrS G:St:R GrSStrSRrS G:St:R Ž. Spring wheat Triticum aesti¨um L. YA 0.23 0.32 1.01 1:1.4:4.4 0.43 0.60 0.60 1:1.4:1.4 MA 0.09 0.19 0.86 1:2:10 0.19 0.21 0.21 1:1:1 WA 0.06 0.18 0.67 1:3:11 0.18 0.35 0.98 1:2:5.4 Ž. Corn Zea mays L. YA 0.23 0.72 0.95 1:3:4 0.27 0.31 0.73 1:1:3 MA 0.10 0.52 0.88 1:5:9 0.17 0.22 0.65 1:1:4 WA 0.06 0.50 0.83 1:8:14 0.10 0.18 0.64 1:2:6 G, grain; St, stem; R, root; S, soil; G:St:R, denotes grain:stem:root. non-ferrous operator effluent did not markedly elevate the soil metal contents in the region stud- ied. Concentrations of trace elements concerned in crop parts showed that the highest concentrations in the two plants occurred in roots, the lowest in seeds. Wheat roots contained 4᎐ 11 times the con- tent found in grains for cadmium, and 1᎐ 5 times for zinc. Corn roots contained 4᎐ 14 times the level discovered in grains for cadmium, and 3᎐ 6 Ž. times for zinc Table 5 . These results agreed with Ž. the previous pot reports of Dudka et al. 1994 , who found that the concentrations of Cd and Zn in spring wheat plant were higher in straw than in grain by factors 3᎐7 and 1.5᎐ 2 for Zn and Cd, Ž. respectively, and Zhou et al. 1994 , who con- firmed that the order of the two element transfer in rice plant from root to tops was root) stem) Ž. grain. Koeppe 1977 pointed out in his review that roots contained at least twice the Cd concen- tration found in tops. The element Cd had a lower transfer ratio compared with the element Zn. It is not surpris- ing about the two trace metals because the ele- ment Zn is essential for plant growth and mobile within the plants, and the most bioavailable metal among the essential trace elements, which probably explains the higher transfer ratios in two Ž. crop plants studied Streit and Stumm, 1993 . The element Cd has not been shown to be essential in plant metabolism, and is probably taken up by the Ž roots and usually confined to the roots Adriano, . 1986 . These results suggested that the roots and stems of the crops studied had a physiological mechanism that prevents grain from excessive Cd and Zn accumulation in edible parts, especially of cadmium because cadmium could be complexed as Cd-binding peptides in roots of several plant Ž. species Mckenna et al., 1993 . As local principal crops, more attention should Ž. be given to edible parts grains . Heavy metal contents in wheat grain at YA and MA were Table 6 y1 Ž. Concentrations of selected heavy metals from the literatures mg kg , DW Element Cd Zn Reference a Ž. Background value Chen 1996 Wheat 0.053 34.6 Corn 0.002 16.6 Maximum safe intake level 0.1 FAOrWHO b Hygienic standards for grain 0.2 50.0 NSBC Ž. Maximum safe intake content 0.3 40.0 Bowen 1979 a The value indicates that in grain in PR China. b Ž. National Standard Bureau of PR China GB15199-94, GB13106-91 . () Z. Nan et al.r The Science of the Total En ¨ironment 285 2002 187᎐ 195 193 either practically identical to or below the back- Ž.Ž ground values BV 0.053 for Cd and 34.6 for Zn, y1 .Ž. mg kg DW reported by Chen 1996 . Only at WA, the contents of cadmium and zinc in wheat grains were significantly higher than the BV, and the level of cadmium in grains was higher than Ž. the hygienic standard in PR China Table 6 . The levels of cadmium in corn grains were 25 and 290 times higher than the BV for YA, MA and WA, respectively. The levels of zinc in corn grains had Ž. the same magnitude with the BV Table 6 . Mea- sures of the trace elements in corn grains were lower than the hygienic standards of PR China except for grain Cd content at WA which was almost 3 times higher than the hygienic standard Ž y1 . 0.2 mg kg , DW . It was clear from the results that crops grown in WA soils appeared to be polluted to some extent. Cd and Zn uptake by the crops studied was well described by four models: linear; exponen- tial; quadratic; and cubic. These results were in accordance with the prevailing assumption that uptake of trace metals by plant structures does not occur in a linear response to contents of the metals in soils, except at a low range of metal concentration in soils. In some researches, Dudka Ž. et al. 1994, 1996 , on the basis of one pot and one field experiment, found that the relationships between Cd and Zn contents of the plant parts Ž. straws and grains and soils were best expressed by exponential equations and power models. In our study, only the relationship between the ele- ment Cd in corn grains and in soils was linear. All correlations between the metals studied in crop tissues and in soils were most significant at P- 0.01, where R values were positive. These data demonstrated that concentrations of crop tissues, metals were dependent on the metal levels in soils. These facts also suggest that the soil total contents of metals are good predictors of soil metal contamination. Interactive effects of multiple metal pollution on plant metal accumulations are common but Ž not consistent Mckenna et al., 1993; Moraghan, . 1993; Zhou et al., 1994; Pichtel et al., 2000 . Most of the findings may be summed up by stating that Zn reduces the uptake of Cd by both root and Ž. foliar system Adriano, 1986 . In the present work, the interaction effects were synergistic, increasing soil zinc strongly elevating crop part cadmium and increasing soil Cd elevating plant tissue Zn in gray calcareous soil when high Cd and Zn con- tents occurred in contaminated soils. These re- sults agreed with the previous reports of Hinsely Ž. et al. 1984 , who reported that repeated sludge applications did result in additional increase of both Cd and Zn contents in corn leaves and grain Ž. in calcareous soils, and Dudka et al. 1994 , who, in their pot experiment, concluded that the con- Ž tents of Cd and Zn in spring wheat parts straw . and grain increased with increasing the two metal concentrations in sandy soils. The present results suggest that in plots highly contaminated with Cd and Zn, soil Zn should not be expected to de- crease Cd significantly in crop parts although there is a strong antagonistic Zn effect on Cd accumulation in plant tissues. Our findings also are in broad agreement with Ž. those of the following reports. Smilde et al. 1992 concluded that Zn and Cd were synergistic to some extent, plant Zn uptake increasing with applied Cd on the basis of interaction experiment Ž. carried out in loam soil in pots. Moraghan 1993 reported that the Cd᎐ Zn effects were synergistic to each other in the presence of added Cd and Cd accumulation in flax seed was reduced by added Ž. Zn in the absence of added Cd. Zhou et al. 1994 concluded from their pot experiment that interac- tion of Cd and Zn resulted in an increase of Cd accumulation and a decrease of Zn uptake in rice plant. The reason for these differences between those results and the work reported here may depend on the Cd and Zn contents and their combinations in soils and also on the soil charac- ters and crop species and tissues. These divergent findings agree with the statement that interaction effects on crop metal uptake in field situations are more difficult to make than in pot or solution Ž. experiments Coughtrey and Martin, 1979 . In following studies we are going to investigate the influence of soil characters on the uptake of elements concerned by the two crops and their transfer in soil crop system in the region studied. () Z. Nan et al.r The Science of the Total En ¨ironment 285 2002 187᎐ 195194 5. Conclusions The translocation ratios of the two metals concerned from soil to crop parts in the region studied were relatively lower, and the order of the element transfer in different plant tissues was root) stem)grain. The transfer ratio of element Cd was lower than that of element Zn. Cd and Zn uptake by the crop structures could be best de- scribed by four models: linear; exponential; quadratic; and cubic. Apart from a linear rela- tionship between element Cd in the corn grains and soils, models were generally non-linear. An analysis of Cd᎐ Zn interaction mechanism led to the conclusion that the effects of the two metals were synergistic to each other, in which increas- ing Cd and Zn contents in soils can increase the accumulations of Zn or Cd in the two crops. Acknowledgements This work was financially supported by Project Ž No. 49731010 from the National Natural Science . Foundation of PR China . 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