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Cadmium phytoavailability to rice (Oryza sativa L.) grown in representative Chinese soils. A model to improve soil environmental quality guidelines for food safety

Cadmium phytoavailability to rice (Oryza sativa L.) grown in representative Chinese soils. A model to improve soil environmental quality guidelines for food safety
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  Cadmium phytoavailability to rice ( Oryza sativa  L.) grownin representative Chinese soils. A model to improve soilenvironmental quality guidelines for food safety Muhammad T. Ra fi q a,b , Rukhsanda Aziz a , Xiaoe Yang a , Wendan Xiao a ,Muhammad K. Ra fi q c , Basharat Ali d , Tingqiang Li a, n a Ministry of Education Key Laboratory of Environmental Remediation and Ecological Health, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China b Department of Environmental Sciences, International Islamic University, Islamabad 44000, Pakistan c Directorate of Range Management and Forestry, Pakistan Agricultural Research Council, Islamabad 44500, Pakistan d College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China a r t i c l e i n f o  Article history: Received 8 July 2013Received in revised form13 October 2013Accepted 16 October 2013 Keywords: Cadmium pollutionHuman dietary toxicityPhytoavailabilitySoil properties Oryza sativa  L  a b s t r a c t Food chain contamination by cadmium (Cd) is globally a serious health concern resulting in chronicabnormalities. Rice is a major staple food of the majority world population, therefore, it is imperative tounderstand the relationship between the bioavailability of Cd in soils and its accumulation in rice grain.Objectives of this study were to establish environment quality standards for seven different texturedsoils based on human dietary toxicity, total Cd content in soils and bioavailable portion of Cd in soil.Cadmium concentrations inpolished rice grainwere best related tototal Cd content in Mollisols and UdicFerrisols with threshold levels of 0.77 and 0.32 mg kg  1 , respectively. Contrastingly, Mehlich-3-extractable Cd thresholds were more suitable for Calcaric Regosols, Stagnic Anthrosols, Ustic Cambosols,Typic Haplustalfs and Periudic Argosols with thresholds values of 0.36, 0.22, 0.17, 0.08 and 0.03 mg kg  1 ,respectively. Stepwise multiple regression analysis indicated that phytoavailability of Cd to rice grain wasstrongly correlated with Mehlich-3-extractable Cd and soil pH. The empirical model developed in thisstudy explains the combined effects of soil properties and extractable soil Cd content on thephytoavailability of Cd to polished rice grain. This study indicates that accumulation of Cd in rice isin fl uenced greatly by soil type, which should be considered in assessment of soil safety for Cdcontamination in rice. This investigation concluded that the selection of proper soil type for food cropproduction can help us to avoid the toxicity of Cd in our daily diet. &  2013 Elsevier Inc. All rights reserved. 1. Introduction Globally, heavy metals present in soil are pollutants, which aretoxic and persistent in nature and have greater impact on humanhealth (Satarug et al., 2003; Cui et al., 2005). Their transfer from both terrestrial and aquatic resources into the food chain adds uptheir accumulation in our consumable food commodities (Grantand Sheppard, 2008). Soil pollution caused by cadmium (Cd) is aserious public health concern as its intake from rice caused Itai-Itaidisease in Japan in 1970s (Kobayashi, 1978). Its uptake by vege-tables or rice from soil is the starting point of exposure pathwayfor human beings (Franz et al., 2008; Kobayashi et al., 2008). Potential dietary risk of high Cd content in soils may be due toeither its enhanced uptake by plants or its competitionwith the Znand Fe resulting in lowering down their concentration as wasfound in Chinese rice (Liu et al., 2003).About 20 percent of agricultural soils in China are contami-nated by heavy metals and Cd pollution accounts for more than1.3  10 5 ha of the total contaminated area (Gu and Zhou, 2002;Du, 2005). The bioaccumulation index of Cd in plants is highrelative to other trace elements, and may exceed many essentialelements due to its greater mobility in soil (Kabata-Pendias andPendias, 2001). Therefore, in terms of food-chain contamination,Cd concentrations in edible parts of the plants need to bemonitored to ensure food safety.Rice ( Oryza sativa  L.) an important cereal crop in globalagriculture, is second (more than 150 million ha) after wheat interms of the planting area of cereal crops. More than 90 percent of the world rice growing area lies in Asia (Kyuma, 2004) mainly inChina. In Asian countries, the contamination of paddy soils byheavy metals is one of the most important issues concerning riceproduction and soil management (Ok et al.,. 2011a). It has been Contents lists available at ScienceDirect journal homepage: Ecotoxicology and Environmental Safety 0147-6513/$-see front matter  &  2013 Elsevier Inc. All rights reserved. n Corresponding author. E-mail address: (T. Li). Please cite this article as: Ra fi q, M.T., et al., Cadmium phytoavailability to rice ( Oryza sativa  L.) grown in representative... . Ecotoxicol.Environ. Saf. (2014), Ecotoxicology and Environmental Safety  ∎  ( ∎∎∎∎ )  ∎∎∎ – ∎∎∎  reported that 1.46  10 8 kg of agricultural products are polluted byCd every year in China; in which 5.0  10 7 kg is only rice (Gu andZhou, 2002; Li et al., 2003). Cadmium content of rice grains was found up to 2.40 mg kg  1 in China ( Jin et al., 2002). In south Korea, the concentration of cadmium in rice grain harvested from metalcontaminated soil near abandoned metal mines was found higherthan food safety guidelines of 0.2 mg Cd kg  1 set by Korean Foodand Drug administration (Ok et al., 2011b).In many regions of theworld, paddy rice is exposed to heavy contaminations of Cd,causing a health hazards. Reports have linked soil Cd pollutionwith human renal tubular dysfunction in subsistence rice farmfamilies (Chaney et al., 2005). Rice is also a leading source of Cd ingestion for the human population in Japan (Tsukahara et al.,2003). In short, paddy rice contaminated by Cd in the soilchallenges the food safety as a whole. Therefore, there are severalissues regarding the environmental quality of soils, food safety andhuman health for the agro-environmental sustainability of worldrice supplies. Actually, a small portion of total trace metals in soil isavailable for plant uptake. It is commonly accepted that the totaltrace metal concentration in soils is neither a good indicator of phytoavailability nor a good tool to assess the potential risk of dietary toxicity (Adriano, 2001; Wang et al., 2004). Water soluble, exchangeable and loosely adsorbed metals are labile and thusavailable to plants (Kabata-Pendias, 1993), and extractable Cdcontent in soil could be a better indicator of bioavailability andtoxicity than the total contents. Cadmium ions can be held on thesoil surface, and the processes involved are dependent on manyfactors including soil composition, pH, redox status, and nature of the contaminant; thus, metal bioavailability and toxicity arevariable among different soils (Tracy and Sheila, 2006). Due to limited number of studies, the environmental qualitystandards of heavy metals in agricultural soils established andapplied in the world are still based on total metal contents of soil.In the past, little attention was given to the difference in metalaccumulation among the edible parts of crops, and the relation-ship between total concentration and phytoavailability of heavymetals (Shentu et al., 2008). Furthermore, the key for improving soil environmental quality guidelines is to develop the tools thatlink the Cd bioavailability in soil with its accumulation in edibleparts. Objectives of this study were to establish soil Cd thresholdsfor representative Chinese soils based on human dietary toxicityand to  fi nd the relationship between soil properties and Cdaccumulation in rice grains. 2. Materials and methods  2.1. Soil collection and analysis Seven typical soils, representing a large diversity of Chinese soils were used forinvestigation in this study. Udic Ferrisols, Mollisols, Periudic Argosols, TypicHaplustalfs, Ustic Cambosols, Calcaric Regosols and Stagnic Anthrosols (ChineseSoil Taxonomy Research Group, 1995) were collected from the cities of Guilin(104 1 40 ′ – 119 1 45 ′ E, 24 1 18 ′ – 25 1 41 ′ N), Harbin (125 1 42 ′ – 130 1 10 ′ E, 44 1 04 ′ – 46 1 40 ′ N),Huzhou (119 1 14 ′ – 120 1 29 ′ E, 30 1 22 ′ – 31 1 11 ′ N), Zhanjiang (110 1 08 ′ – 110 1 77 ′ E, 20 1 33 – 21 1 62N), Qufu (116 1 51 ′ – 117 1 13 ′ E, 35 1 29 ′ – 35 1 49 ′ N), Ya'an (102 1 37 ′ – 103 1 12 ′ E,29 1 23 ′ – 30 1 37 ′ N) and Jiaxing (120 1 7 ′ – 121 1 02 ′ E, 30 1 5 ′ – 30 1 77 ′ N) respectively.All soils were drawn from the same upper horizon (0 – 20 cm). After removal of visible pieces of plant materials, grit, earthworms, etc., the soil samples were air-dried, ground, and screened through a 2 mm sieve. All the soils were analyzed forpH (Chaturvedi and Sankar, 2006), cation exchange capacity (Hendershot and Duquette, 1986), organic matter contents (Rashid et al., 2001), and particle size density (Day, 1965). Relevant physicochemical properties of these soils are shown in Table S1.  2.2. Cd spiking  Samples of Mollisols, Periudic Argosols, Stagnic Anthrosols and Ustic Cambo-sols with the background values (BV) of Cd concentration below 0.50 mg kg  1 werespiked with Cd as Cd(NO 3 ) 2  in an aqueous solution at loading rates of 1.0, 2.0, 4.0,6.0 and 8.0 mg Cd kg  1 soil along with a no Cd loading control (Ck). On the otherhand, the soil samples of Udic Ferrisols, Typic Haplustalfs and Calcaric Regosols,with the background values (BV) of Cd concentration above 0.50 mg kg  1 , werespiked with Cd to establish the contamination levels of 2.0, 4.0, 6.0 and8.0 mg Cd kg  1 soil along with Ck. Distilled water was added to adjust the soilmoisture to 70 percent of its water-holding capacity. All the spiked soil sampleswere aged for six months prior to pot experiments. At the end of six months agingperiod, concentrations of total and Mehlich-3-extractable Cd were determined inall the treated soils.  2.3. Green house experiment  A greenhouse experiment was conducted by growing rice in pots during June  – October, 2011 at Zhejiang University, Hangzhou, PR China. The rice ( Oryza sativa L .)variety used was Zhongzheyou 1, being a single season indica variety with anaverage plant height of 120 cm. This long duration variety takes about 140 days tomature. Seed of the variety was obtained from the Zhejiang Seed Co. Seeds weresurface sterilized by washing with 70 percent ethanol for 1 min and soaking in0.01 g mL   1 sodium hypochlorite for 5 min, rinsed thoroughly in deionized water,and then imbibed in deionized water for 48 h at 30  1 C (Wu et al., 2011). Then seeds were germinated in quartz sand washed with 5 percent (v/v) HCl. Rice seedlings(aged about 30 days) were transplanted in plastic pots having 20 cm diameter and20 cm height, each containing 5 kg soil. All the treatments were conducted intriplicate under a completely randomized design. Fertilizers were applied (per pot)as basal dressing at the rates of 0.5 g of N as (NH 4 ) 2 S0 4 , 0.12 g of P 2 O 5  as SSP (singlesuper phosphate), and 0.6 g of K 2 O as K 2 S0 4 . A Second dose of ammonium sulfate astop dressing was also applied at the rate of 0.5 g of N per pot at 60th day aftertransplanting. Plants were grown under  fl ooding conditions from transplanting tillmaturity.  2.4. Soil and rice grain analysis 2.4.1. Grain sample collection and preparation Rice plants were harvested from each pot at maturity and were manuallythreshed to separate grains. Then air dried to constant weights, and processedaccording to  “ The Testing Methods of Rice Qualities ”  published by Chinese Ministryof Agriculture (NY147-88). Husk from the rice grains was removed by using alaboratory de-husker (OHYA-25, Japan), and the brown rice was polished with arice polishing machine (CPC 96-3, China) until the cortex (embryo) was removedfrom the brown rice. The polished rice samples were ground to make powder in aball mill (Retsch, MM-301, Germany).  2.4.2. Total Cd of soil and polished rice After rice harvesting, the soil samples were collected from each pot, thoroughlymixed and air-dried; sub-samples of soil were ground to  o 0.149 mm using anagate mill for total Cd determination. For analysis of total Cd in soil, 0.20 g of ground soil sample was digested with a mixture of HNO 3  (5 mL), HClO 4  (1 mL) andHF (1 mL) (Shentu et al., 2008). For grain samples, 0.30 g of rice powder was put into the digestion tubes and digested with HNO 3  (5 mL) and H 2 O 2  (1 mL). Aftercooling, resultant solutions were diluted to 25 mL using two percent HNO 3  andthen  fi ltered (Shentu et al., 2008). Cadmium concentrations in the  fi ltrate weredetermined using inductively coupled plasma-mass spectrometry (ICP-MS, Agilent,7500a,) following a standard procedure. The same procedure without samples wasused as control and three replications were conducted for each sample. Qualityassurance and quality control (QA/QC) for Cd in soil and rice grainwas estimated bydetermining Cd contents in the standard reference materials (soil GSBZ 50013-88and rice NCSZC 73008) respectively, approved by General Administration of QualitySupervision, Inspection and Quarantine of the People's Republic of China (AQSIQ),with a recovery rate of 96.5 percent and 101.2 percent respectively.  2.4.3. Mehlich-3-extractable Cd in Soils Mehlich-3-extractable Cd in soils was determined following the extractionmethod described by Mehlich (1984). Brie fl y, 5 g (0.2 mm sieved) of dry soil wasshaken with 50 mL of Mehlich-3 solution (0.2 mol L   1 CH 3 COOH, 0.25 mol L   1 NH 4 NO 3 , 0.015 mol L   1 NH 4 F, 0.013 mol L   1 HNO 3 , 0.001 mol L   1 EDTA) for 5 min(200 rpm) at 25  1 C, and then the suspension was centrifuged at 5000 rpm for10 min and  fi ltered through 0.45  μ m  fi lter paper. The same procedure withoutsamples was used as control and three replications were conducted for eachsample. The Cd concentration in the  fi ltrate was analyzed by ICP-MS (Agilent,7500a, Agilent Technologies, CA, USA). Quality assurance and quality control (QA/QC) for extractable Cd in soil was estimated by determining Cd contents in thestandard reference material (soil GBW 07443GSF-3), approved by General Admin-istration of Quality Supervision, Inspection and Quarantine of the People's Republicof China (AQSIQ), with a recovery rate of 97.6 percent. M.T. Ra  fi q et al. / Ecotoxicology and Environmental Safety  ∎  ( ∎∎∎∎ )  ∎∎∎ – ∎∎∎ 2 Please cite this article as: Ra fi q, M.T., et al., Cadmium phytoavailability to rice ( Oryza sativa  L.) grown in representative... . Ecotoxicol.Environ. Saf. (2014),   2.5. Statistical analysis One-way analysis of variance (ANOVA), linear regression and multiple regres-sion analyses were performed using the statistical software package SPSS (version18.0). Means of data were compared by least signi fi cant difference (LSD) test at  fi vepercent signi fi cance level. 3. Results and discussion  3.1. Characteristics of soils Soils in this study are representative of the majority of Chinesesoils and tend to be strongly acidic to mild alkaline. There weresigni fi cant differences in the physico-chemical properties amongthe seven soils (Table S1) for in fl uencing the Cd accumulation inrice grain. Total Cd and Zn concentrations (background value)in the soils ranged from 0.47 to 1.06 mg kg  1 and 5.10 to34.08 mg kg  1 , respectively. Soil pH ranged from 4.43 for the UdicFerrisols to 8.02 for the Calcaric Regosols, viz., strongly acidic tomild alkaline, total organic matter content from 7.54 g kg  1 inthe Ustic Cambosols to 32.19 g kg  1 in Mollisols, and cationexchange capacity from 12.6 cmol kg  1 for the Periudic Argosolsto 34.0 cmol kg  1 for the Mollisols. The clay contents ranged fromthirteen percent in Ustic Cambosols to 49.6 percent in UdicFerrisols, and silt fractions ranged from 39.8 percent in UdicFerrisols to 73.0 percent in Stagnic Anthrosols.  3.2. Mehlich-3-extractable Cd in soils after aging of six months Mehlich-3 extractable Cd content increased signi fi cantly withincreasing Cd spiking levels in all the seven soils (Table S2).Mehlich-3-extractable Cd was found in range of 0.16 – 5.10 mg kg  1 in these soils under different Cd levels. The Cd contents variedsigni fi cantly among these soils, decreasing in order: Typic Hap-lustalfs 4 Udic Ferrisols 4 Periudic Argosols 4 Ustic Cambosols 4 Mollisols 4 Stagnic Anthrosols 4 Calcaric Regosols. Percentincrease in Mehlich-3-extractable Cd was greater at higher ratesof Cd application in each soil. These results showed that minimumand maximum extractability was in Ya'an soil (Calcaric Regosols)and Zhanjiang soil (Typic Haplustalfs), respectively under thehighest level of Cd applied (8 mg kg  1 ).  3.3. Biomass yield of rice Different Cd loading rates signi fi cantly in fl uenced the grainbiomass of rice in various soils (Table 1). Lower levels of Cd hadstimulatory effect on grain yield of rice in Mollisols, TypicHaplustalfs, Stagnic Anthrosols, and Udic Ferrisols. The dryweights of rice decreased gradually as the Cd concentrationincreased in all soils as compared to control. This decrease in dryweight was 11.7, 20.1, 45.2, 168.5, 92.7, 44.2 and 24.3 percent inMollisols, Ustic Cambosols, Stagnic Anthrosols, Periudic Argosols,Udic Ferrisols, Typic Haplustalfs and Calcaric Regosols, respectivelyat 8 mg kg  1 Cd level as compared totheir respective controls. Thedry weight of rice grain at 8 mg kg  1 generally decreased in order:Mollisols 4 Calcaric Regosols 4 Ustic Cambosols 4 Stagnic Anthro-sols 4 Typic Haplustalfs 4 Udic Ferrisols 4 Periudic Argosols.Reduction in biomass might be due to the adverse effects of Cdon the roots, so plants were not able to take up nutrients andcontinue their normal activity. It has been well documented thatCd can suppress plant growth by interfering in various metabolicprocesses, inhibition of the proton pump, reduction of rootelongation, and damage to photosynthetic machinery (Aidid andOkamoto, 1993; Ali et al., 2013a,b). Moya et al. (1993) also stated that excess amount of Cd in soil could cause disturbances inmineral nutrition and carbohydrate metabolism. It has beenpreviously found 25 percent loss in yield with application of Cdat 4 – 5 ppm concentration in spinach and soybean under soilconditions (Bingham,1979). Our results conform with the  fi ndingsof  John et al. (1972), who observed that Cd at 100 ppm decreased root and shoot weight by 67 and 47 percent, respectively, in radishin 30 different soils. Sadana and Singh (1987) found 23 percentloss in growth of lettuce by adding 4 ppm Cd in loamy sand soil.  3.4. Accumulation of Cd in polished rice grain Cadmium at different concentrations signi fi cantly affected Cdaccumulation in polished rice grains obtained from seven soils(Fig. 1). There was a wide range in rice grain Cd concentrations,with values ranging between 0.0 and 12.5 mg kg  1 DW. Cadmiumcontents in polished rice grain varied with Cd levels and type of soil, and it enhanced with increasing level of Cd in each soil. Thelowest and highest Cd contents were observed at higher level of Cd (8 mg kg  1 ) in Calcareous and Periudic Argosolss, respectively.Cadmium accumulation in polished rice grain was found signi fi -cantly different due to difference in Cd phytoavailability amongthe seven soils. Cadmium concentrations in rice followed an orderof Periudic Argosols 4 Typic Haplustalfs 4 Udic Ferrisols 4 UsticCambosols 4 Mollisols 4 Stagnic Anthrosols 4 Calcaric Regosols at8 mg kg  1 Cd level. The Cd concentrations in polished rice grainranged from 2.52 to 12.50 mg kg  1 at higher level of Cd(8 mg kg  1 ) in all soils.Variations of Cd accumulation in polished rice grain in differentsoils could be due to difference in Cd phytoavailability in each soildiffering in soil pH. Bingham et al. (1980) stated that Cd content of rice grain was highly dependent upon the soil pH being highest atpH 5.5. Moreover, similar  fi ndings were found by Ok et al. (2011a,b) in rice grown under Cd contaminated soils when addedamendments altered soil pH. Kim and Kim (1980) found that Cdcontents in brown rice were up to 0.35 mg kg  1 fresh weight withthe application of soil Cd at 5 mg kg  1 . Cadmium contents in grainshoot and root increased about four to six, two to  fi ve and four tonine fold, respectively, at 9 mg kg  1 soil Cd treatment in clay loamsoil (Kibria et al., 2006).  Table 1 Dry weight (g pot  1 ) of rice grown on representative Chinese soils with different loading rates of Cd.Cd level (mg kg  1 ) Mollisols Ustic Cambosols Stagnic Anthrosols Periudic Argosols Typic Haplustalfs Udic Ferrisols Calcaric RegosolsCk 46.82 7 1.33b 36.40 7 1.76b 35.71 7 0.59c 34.07 7 0.58a 31.19 7 1.03a 32.74 7 1.03b 45.68 7 1.32a1.0 42.99 7 0.50cd 33.84 7 2.12b 38.96 7 1.46b 33.26 7 1.67b  – – – 2.0 44.96 7 2.06bc 41.94 7 1.97a 41.88 7 1.10a 31.46 7 1.23b 27.44 7 1.08b 35.16 7 1.48a 41.22 7 1.78bc4.0 50.33 7 0.84a 35.47 7 0.94b 35.93 7 1.08c 28.12 7 0.78c 20.58 7 1.23d 27.18 7 0.90c 42.79 7 0.90b6.0 45.41 7 2.16bc 34.03 7 1.74b 27.29 7 1.71d 28.39 7 1.12c 25.03 7 1.14c 24.99 7 1.01d 39.53 7 1.25c8.0 41.33 7 0.78d 30.32 7 1.41c 24.60 7 1.06e 12.69 7 0.93d 17.41 7 1.28e 16.99 7 0.99e 34.56 7 1.15dMean values followed by different letters within the same column are signi fi cantly different at  P  o 0.05. M.T. Ra  fi q et al. / Ecotoxicology and Environmental Safety  ∎  ( ∎∎∎∎ )  ∎∎∎ – ∎∎∎  3 Please cite this article as: Ra fi q, M.T., et al., Cadmium phytoavailability to rice ( Oryza sativa  L.) grown in representative... . Ecotoxicol.Environ. Saf. (2014),   3.5. Relationship between Mehlich-3-extractable Cd in soilsand grain Cd content  Mehlich-3 extractant seemed ef  fi cient to evaluate Cd phytoa-vailability to polished rice grain, grown in seven different texturedsoils (Table 2), as evidenced by high correlation coef  fi cients( R 2 4 0.96). It is in agreement with our recent studies (Xiaoet al., 2013a,2013b), which re fl ected high linear correlations( R 2 4 0.98) between Mehlich-3-Cr and Cr contents in rice grainand pak choi under different soil types. Our  fi ndings are alsoconform to the observations of  Bhattacharyya et al. (2005) whoreported that extractable metal was a good soil test index formetals phytoavailability in rice crop. In fact, the Mehlich-3extraction method is applicable to a wide range of soil pH, fromacidic to alkaline (De Villiers et al., 2010), which makes it ideal for application at countrywide scale as the case in our study. Princi-pally, the extraction methods are based on the assumption thatthere is a relationship between the extractable fraction of metalsand the phytoavailability of the metals to plants (Wang et al.,2004). Kabata-Pendias (1993) reported that Mehlich-3 extractable Fig.1.  Cadmium contents (mg kg  1 DW ) in polished rice grain grown under different Cd concentration in Mollisols (A), Ustic Cambosols (B), Stagnic Anthrosols (C), PeriudicArgosols (D), Typic Haplustalfs (E), Udic Ferrisols (F) and Calcaric Regosols (G).  Table 2 Regression correlation between Cd contents in the polished rice grain and differentforms of Cd in various soils.Soil type Form of soil Cd Regression equation  R 2 Mollisols Total Cd  Y  ¼ 0.4721  x  0.1926 0.9931Melich-3 extractable Cd  Y  ¼ 0.8928  x  0.0471 0.9875Ustic Cambosols Total Cd  Y  ¼ 0.7239  x  0.3687 0.9884Melich-3 extractable Cd  Y  ¼ 1.4051  x  0.0634 0.9951Stagnic Anthrosols Total Cd  Y  ¼ 0.4251  x  0.1874 0.9605Melich-3 extractable Cd  Y  ¼ 0.8175  x  0.0078 0.9932Periudic Argosols Total Cd  Y  ¼ 1.5094  x  0.1531 0.9592Melich-3 extractable Cd  Y  ¼ 2.4612  x þ 0.0978 0.9682Typic Haplustalfs Total Cd  Y  ¼ 1.5476  x  0.4495 0.9737Melich-3 extractable Cd  Y  ¼ 2.196  x  0.0008 0.9825Udic Ferrisols Total Cd  Y  ¼ 1.4588  x  0.3016 0.991Melich-3 extractable Cd  Y  ¼ 2.2496  x þ 0.0244 0.9851Calcaric Regosols Total Cd  Y  ¼ 0.3364  x  0.2605 0.9831Melich-3 extractable Cd  Y  ¼ 0.6584  x  0.0623 0.9924 M.T. Ra  fi q et al. / Ecotoxicology and Environmental Safety  ∎  ( ∎∎∎∎ )  ∎∎∎ – ∎∎∎ 4 Please cite this article as: Ra fi q, M.T., et al., Cadmium phytoavailability to rice ( Oryza sativa  L.) grown in representative... . Ecotoxicol.Environ. Saf. (2014),  metals, such as soluble, exchangeable, and looselyadsorbed metalsare quite labile and readily available for plants.  3.6. Multiple regression model for predicting cadmium phytoavailability to polished rice Cadmium uptake by plants is in fl uenced by physical, chemical,and biological mechanisms, therefore, combinations of these basicsoil properties may explain Cd uptake by plants (McBride, 2002). Concentration of Zn can affect Cd uptake by plants, presumablydue to competition between these two metals for uptake andtransport inside the plant (Oliver et al., 1994; Welch et al., 1999). With this consideration, soil pH, OM, CEC, total soil Zn, total soilCd, Mehlich-3-extractable Cd, and clay content were integrated tosimulate the combined effects of rhizosphere environment on Cdphytoavailability to rice grains. Stepwise regression analysis wasused and two independent variables Mehlich-3-extractable Cdcontent and pH were extracted as being signi fi cant (Table 3). Bothcoef  fi cients of multiple correlation and partial regression reachedat least the 0.05 statistically signi fi cant levels. For multiple linearregressions,  R  2 values can be used to explain variation of thedependents (Wang et al., 2004). Table 3 showed that both  R  2 values were above 0.93, which means that more than 93 percentof variation in Cd concentration of polished rice grain can beattributed to soil Mehlich-3-extractable Cd content and pH.Coef  fi cients of each in fl uencing factor can be used to indicate thein fl uencing ability of these factors (Wang et al., 2004). A close relationship was noticed while comparing the observed Cd in ricegrain and Cd concentrations predicated by this model (Fig. S1).Recommended model suggested that Cd concentration in thepolished rice grain was enhanced by higher soil Mehlich-3-extractable Cd content, and lower soil pH (positive coef  fi cientsshowed positive effect and vice versa). Mehlich-3-extractable Cdfractions are assumed to be easily absorbed fractions by plants,lower pH is among the factors which enhance the bioavailabilityCd contents in soils; therefore, these two variables gave thecontradictory effect on Cd phytoavailability. Wang et al. (2004)found that soil properties (e.g., OM content, pH, and CEC) affectedthe phytoavailability of metals in soils, and such in fl uences thus beconsidered in the evaluation of metal phytoavailability. Among thetwo parameters involved in this model, interactions between themwere obvious (e.g., Cd concentration in the extractable fractionwas correlated with lower soil pH) (Table S2). Furthermore, thecoef  fi cients obtained in this model can regulate these cross effectsand make a better model  fi tting. For example, although there wasa negative correlation between the soil Mehlich-3-extractable Cdconcentrations and pH, these two factors had a contradictoryeffect on Cd phytoavailability and the Mehlich-3-extractable Cdconcentration was the leading factor in fl uencing Cd phytoavail-ability to polished rice grain (the coef  fi cient of Mehlich-3-extractable Cd was positive and greater than pH). These resultsare in accordance with the  fi nding of  Wang et al. (2004) whodeveloped an empirical model to correlate the Cd phytoavailabilityto celery with common soil properties, total and extractable Cdconcentrations of soil. They found that soil-extractable Cd wasleading factor in fl uencing Cd phytoavailability, with pH, alsohaving an in fl uence; however total soil Cd concentration andorganic matter contents were not included in model  fi tting.  3.7. Soil Cd thresholds for potential dietary toxicity in rice For ensuring the environmental and food safety, an effort wasmade to develop guidelines for acceptable concentrations of potentially harmful Cd in seven different agricultural soils of China. In this regard, the factor needs to be considered is; theconcentration of Cd in polished rice above which food safety forhuman beings is negatively affected. Since, Cd phytoavailabilitydiffered among soil types, the focus was on the development of soil Cd thresholds for representative Chinese soils based on foodsafety. According to the FAO/WHO Joint Expert Committee on FoodAdditives, Provisional Tolerable Weekly Intake (PTWI) of Cadmiumis 7  μ g kg  1 of body weight (FAO/WHO, 2003). Daily intake of metal (DIM) was determined by the following equation. DIM  ¼ C  cadmium  D food intake B average weight Where,  C  cadmium ,  D food intake  and  B average weight  represent average Cdconcentration in polished rice (mg kg  1 ), daily intake (g) and bodyweight (kg) of the adults, respectively. Average daily intake of ricefor adults was considered to be 323 g person  1 day  1 (Zhonget al., 2006). Average body weight of adult was considered to be55.9 kg as used in previous studies (Ge, 1992; Wang et al., 2005). According to the above equation of DIM, the provisional tolerabledaily intake of Cd for polished rice was 0.173 mg kg  1 on a dryweight basis. Soil Cd thresholds for potential dietary toxicity of polished rice were calculated according to the tolerable dailydietary level of cadmium (0.173 mg kg  1 ), the regression equa-tions in Table 2, and these results are shown in Table 4. Cadmium concentrations in rice grainwere signi fi cantly relatedto total Cd and Mehlich-3-extractable Cd contents in soils, with  R  2 values of 0.959 to 0.993, and 0.968 to 0.995, respectively. Total Cdthresholds for potential dietary toxicity conformed an orderCalcaric Regosols 4 Stagnic Anthrosols 4 Mollisols 4 Ustic Cambo-sols 4 Typic Haplustalfs 4 Udic Ferrisols 4 Periudic Argosols andwere 1.29, 0.85, 0.77, 0.75, 0.40, 0.32 and 0.21 mg kg  1 , respec-tively. Mehlich-3-extractable Cd thresholds decreased in thefollowing order: Calcareous 4 Mollisols 4 Stagnic Anthrosols 4 Ustic Cambosols 4 Typic Haplustalfs 4 Udic Ferrisols 4 PeriudicArgosols and were 0.36, 0.25, 0.22, 0.17, 0.08, 0.07 and0.03 mg kg  1 , respectively. From this investigation, Cd concentra-tions in rice grain were best related to total Cd content in Mollisolsand Udic Ferrisols with the threshold levels of 0.77 and  Table 3 Stepwise regression model for predicting Cd concentration ( Y  ) in polished ricegrain based on soil characteristics. R 2 F   value  T   value and  R 2 of partialregression coef  fi cient T   value  R 2 Y  ¼ 5.14 þ 4.73 Cd Ext  1.5 pH 0.933 27.7 nn Cd Ext  2.84 n 0.669pH   2.81 n 0.666Cd Ext  refers to Mehlich-3 extractable cadmium content. n Indicates signi fi cant levels of probability at 0.05. nn Indicates signi fi cant levels of probability at 0.01.  Table 4 Soil cadmium threshold levels for potential dietary toxicity in polished rice graincalculated from the permissible limit of Cd in rice grain and regression equations inTable 4.Soil type Total Cd (mg kg  1 ) Melich-3 extractable Cd (mg kg  1 )Mollisols 0.77 0.25Ustic Cambosols 0.75 0.17Stagnic Anthrosols 0.85 0.22Periudic Argosols 0.21 0.03Typic Haplustalfs 0.40 0.08Udic Ferrisols 0.32 0.07Calcaric Regosols 1.29 0.36Permissible limit of Cd in rice grain ¼ 0.173 mg kg  1 dry weight. M.T. Ra  fi q et al. / Ecotoxicology and Environmental Safety  ∎  ( ∎∎∎∎ )  ∎∎∎ – ∎∎∎  5 Please cite this article as: Ra fi q, M.T., et al., Cadmium phytoavailability to rice ( Oryza sativa  L.) grown in representative... . Ecotoxicol.Environ. Saf. (2014),
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