Arsenic toxicity in four different varieties of Rice (Oryza sativa L.) of West Bengal, India

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1 Arsenic toxicity in four different varieties of Rice (Oryza sativa L.) of West Bengal, India Piyal Bhattacharya 1,2,, A. C. Samal 1, J. Majumdar 1, S. Banerjee 1, S. C. Santra 1 1 Department of Environmental Sc., University of Kalyani, W. Bengal, India 2 Kanchrapara College, North 24 Parganas, West Bengal, India piyal_green@yahoo.co.in Abstract A green hose pot experiment was conducted on three widely cultivated high yielding varieties of rice namely Ratna, IR 50 and Gangakaveri and on one local rice variety (Tulsa) of West Bengal, India to investigate the uptake and distribution of arsenic in the different fractions of the rice plant. 5.0, 10.0, 20.0, 30.0 and 40.0 ppm or mg kg -1 dry weight of arsenic dosing (in the form of sodium arsenate, Na 2 HAsO 4 ) was applied to study the arsenic phytotoxicity in rice. The results showed that the uptake of arsenic in the rice plant varied with the different rice varieties. With the increasing concentrations of arsenic added to pot soil, the accumulation of arsenic in the rice grain was found to increase, but not necessarily in the same rate. The high yielding rice varieties were found to be higher accumulator of arsenic as compared to the studied local rice variety, Tulsa. Irrespective of the rice varieties, arsenic accumulated mostly in the root of the rice plant, followed by accumulation in the straw, husk and grain parts. In most of the rice varieties, the accumulation of arsenic in the rice grain was found to exceed the WHO recommended permissible limit in rice (1.0 mg kg -1 dry weight) at the 20.0 mg kg -1 arsenic dosing in pot soil, which is very near to the reported arsenic content of West Bengal soil (19.4 mg kg -1 dry weight). In that scenario if not mitigated, consumption of arsenic-contaminated rice will become another potent route of entrance of arsenic toxicity in the human food chain along with the present drinking water pathway. Keywords: Arsenic accumulation, Arsenic pollution, Arsenic toxicity, Rice (Oryza sativa L.), West Bengal. 1. Introduction Arsenic is a naturally occurring toxic metalloid, which can be found in all living materials, as well as in the air, soil and water. The intake of arsenic by humans occurs through contaminated water and food. The epidemiological studies show that the chronic arsenic poisoning can cause serious health effects including cancers, melanosis (hyper pigmentation or dark spots and hypo pigmentation or white spots), hyperkeratosis (skin hardening), restrictive lung disease, peripheral vascular disease (black foot disease), gangrene, diabetes mellitus, hypertension and ischemic heart disease (Guha-Mazumder et al. 2000; Srivastava et al. 2001; Rahman 2002). According to Lehoczky et al. (2002) and Norra et al. (2005) the uptake of arsenic by agricultural plants is a function of availability of arsenic (content, water requirement, soil properties) as well as physiological properties. Several crop plant species (rice, elephant foot yam, green gram, arum, amaranth, radish, lady s finger, cauliflower, Brinjal, etc.) are reported to accumulate arsenic in substantial quantities (Duxbury et Page 99

2 al. 2003; Norra et al. 2005; Rahman et al. 2007; Dahal et al. 2008; Meharg et al. 2009; Bhattacharya et al. 2010a,b; Roberts et al. 2010). A few works had been previously done to analyze the effect of arsenic on different varieties of rice plant (Alam et al. 2003; Rahman et al. 2007,2008). In green house pot experiments with the higher concentrations of arsenic in soil, different rice varieties have showed significant differences in the accumulations of arsenic in straw, husk and grain parts (Alam et al. 2003; Rahman et al. 2007). Analyzing the two widely cultivated rice varieties in Bangladesh, Rahman et al. (2007) reported that the BRRI dhan 28 and BRRI hybrid dhan 1 had differed in the amount of arsenic accumulation (0.5 ± 0.0 and 0.6 ± 0.2 mg kg -1 dry weight of arsenic, respectively). Rahman et al. (2008) by studying five different hybrid as well as non-hybrid rice samples reported that the arsenic translocation from root to shoot (straw) and husk was higher in the hybrid variety BRRI hybrid dhan 1 compared to those of non-hybrid varieties (BRRI dhan 28, BRRI dhan 29, BRRI dhan 35 and BRRI dhan 36). Bhattacharya et al. (2010a) observed relatively higher translocation ( ) of arsenic in the Red Minikit (a high yielding variety of rice) compared to the translocation ( ) by a local rice variety, Megi. In West Bengal (India) groundwater arsenic contamination is in alarming condition for long. Over 50 million people living in the Ganga-Meghna-Bramhaputra plain are at the risk through severe arsenic toxicity. Nine out of total nineteen districts of West Bengal has groundwater arsenic contamination (Bhattacharya et al. 2010a,b). In the rural areas of West Bengal arsenic-contaminated groundwater is not only used for drinking purpose, but also used for irrigation of various crops and especially for rice. Samal et al. (2010) and Bhattacharya et al. (2010b) in their studies on arsenic accumulation in crops of West Bengal concluded that if the common trend of using arsenic-contaminated groundwater for irrigation continues, there is a high possibility of increase of arsenic levels in the crops, including rice in near future. Thus a green house pot experiment was conducted on three widely cultivated high yielding varieties of rice namely Ratna, IR 50 and Gangakaveri and on one local rice variety (Tulsa) of West Bengal to investigate the uptake and distribution of arsenic in the different fractions of the rice plant. This study would help to find rice varieties which are resistant to arsenic phytotoxicity. 2. Materials and methods 2.1 Description of experimental site The pot culture experiment of rice (Oryza sativa L.) was conducted in a glass house at Department of Environmental Science, University of Kalyani, West Bengal, India campus. This experiment site had good sunshine throughout the day. The climate of this area is sub-tropical and humid, characterized by high temperatures during March June, high rainfall during the monsoon season (July-October) and low temperatures during winter (November February). Though the experiment was conducted in glass house, the environmental conditions inside the glass house were not controlled strictly throughout the experiment. Normal environmental conditions were maintained inside the glass house. The glass house was only used to protect the experiment from some unwanted disturbances. Therefore, the conditions inside the glass house did not differ from that of out side. Page 100

3 2.2 Soil collection and pot preparation Soil was collected from University of Kalyani campus at a depth of 0-15 cm. After collection, the soil was sun dried for 7 days and massive aggregates were broken by gentle crushing. The unwanted materials such as dry roots, grasses, hard stones were removed and the soil was made homogeneous. Large earthen pots (43X40 cm) were used for rice cultivation. The pots were designed to be pore less for preventing loss of water soluble arsenic from pots. About 10 kg of soil was taken in a series of earthen pots. There were, in total, 72 pots comprising five different arsenic treatments (5.0, 10.0, 20.0, 30.0 and 40.0 mg kg -1 dry weights, on a soil weight basis) along with one control treatment (no arsenic dosing), each with three replications for the four different rice plant varieties. The arsenic was applied in the form of sodium arsenate, Na 2 HAsO 4, which can easily convert into arsenite form under the reducing and submerged condition of paddy soil. After the application of arsenic, soils were left in the pots for 2 days without irrigation. Then arsenic-free tap water was used to irrigate the pots to make the soil clay suitable for rice seedling transplantation. About 3 4 cm water from the soil level was maintained in the pot before seedling transplantation. After transplantation, 3 4 cm water from soil level was maintained in each pot throughout the growth period by irrigating with arsenic-free tap water. Irrigation was stopped before 10 days of harvest. 2.3 Selection of rice varieties and seedling transplantation Three high yielding varieties (Ratna, IR 50 and Gangakaveri) and one local variety of rice (Tulsa), highly cultivated in West Bengal were selected through germination test for in-vitro green-house pot experiment. Seedlings of 35 days old were carefully uprooted from seedbed and transplanted in flooded condition. Eight seedlings, 6 in. apart from each other, were transplanted in each pot. The seedlings, which died within 7 days of transplantation, were discarded and were replaced by new seedlings. 2.4 Sample collection and preservation The full-grown rice plants were carefully uprooted and rice grain was harvested at their maturity stage ( days after transplantation). Then the collected samples were washed thoroughly with arsenic-free water to remove soil and other contaminants followed by rinsing with de-ionized water with continuous shaking for several minutes. Finally, the samples were dried in the hot air oven at 60 O C for 72 h and were stored in airtight polyethylene bags at room temperature with proper labeling. Proper care was taken at each step to minimize any sort of contamination. 2.5 Sample digestion Samples were digested following heating block digestion procedure (Rahman et al. 2007). 0.5 g of the sample was taken into clean dry digestion tubes and 5 ml of concentrated HNO 3 was added to it. The mixture was allowed to stand over night under fume hood. In the following day, the digestion tubes were placed on a heating block and heated at 60 o C for 2 h. The tubes were then allowed to cool at room temperature. Then 2 ml of concentrated HClO 4 was added and the tubes were again heated at 160 o C for about 4-5 h. The heating was stopped when the dense white fume of HClO 4 was emitted. The content was Page 101

4 then cooled, diluted to 25 ml with de-ionized water and filtered through Whatman No. 41 filter papers and finally stored in polyethylene bottles. Prior to sample digestion all glass goods were washed with 2% HNO 3 followed by rinsing with de-ionized water and drying. 2.6 Sample analysis The total arsenic of samples was analyzed by flow injection hydride generation atomic absorption spectrophotometer (FI-HG-AAS, Perkin Elmer AAnalyst 400) using external calibration (Welsch et al. 1990). The optimum HCl concentration was 10% v/v and 0.4% NaBH 4 produced the maximum sensitivity. For each sample three replicates were taken and the mean values were obtained on the basis of calculation of those three replicates. Standard Reference Material (SRM) from National Institute of Standards and Technology (NIST), USA were analyzed in the same procedure at the start, during and at the end of the measurements to ensure continued accuracy. 3. Results and discussion 3.1 Analytical quality control data The observed arsenic concentration (mg kg -1 dry weight) of SRM Rice Flour (1568A) from NIST, USA was 0.27 ± 0.08 (certified value 0.29 ± 0.03). The certified and the observed values were thus in good agreement. 3.2 Arsenic accumulation in different parts of rice plant The fractional distribution of soil arsenic contents on different parts of the rice plants of four different varieties viz. Tulsa, Ratna, IR 50 and Gangakaveri are shown in Table 1. An important finding from the results is that the uptake of arsenic in the rice plant varied with the four different rice varieties. From various previously conducted in-vivo studies (Bhattacharya et al. 2010a,b; Samal et al. 2010) the average concentration of arsenic in the paddy field soil of West Bengal was found to be just below the global average level of arsenic in agricultural field soil (10.0 mg kg -1 ) (Das et al. 2002). So, the comparison of arsenic accumulation in the grain of the different rice varieties at 10.0 mg kg -1 show that IR 50 and Gangakaveri are high accumulator of arsenic (0.87 ± ± 0.03 mg kg -1 dry weight) as compared to the other two rice varieties Tulsa and Ratna, with much lower accumulation of arsenic (0.41 ± ± 0.03 mg kg -1 dry weight). The high accumulator IR 50 and Gangakaveri are the two high yielding varieties (HYV) of rice while low accumulator Tulsa is a local rice variety and Ratna is a HYV of rice. At this concentration of arsenic dosing in pot soil (10.0 mg kg -1 ) the accumulation of arsenic in rice grain in any of the studied sample did not exceed the WHO recommended permissible limit in rice (1.0 mg kg -1 ) (Abedin et al. 2002; Rahman et al. 2007). But with the increasing concentration of arsenic added to the pot soil, the accumulation of arsenic in the rice grain was also found to increase, but not necessarily in the same rate (Table 1). At the maximum level of arsenic dosing in pot soil (40.0 mg kg -1 ), comparison of arsenic accumulation in grain of the different rice varieties show that IR 50 and Gangakaveri still remain as higher accumulator of arsenic (1.99 ± ± 0.18 mg kg -1 dry weight) as compared to the Tulsa rice variety with accumulation as low as 0.50 ± 0.08 mg kg -1 dry weight of arsenic. Apart from Tulsa the accumulation of arsenic in the rice grain of other three rice varieties was found to cross the WHO recommended permissible limit in rice (1.0 mg kg -1 ) at 20.0 mg kg -1 arsenic dosing in pot soil. The highest content of arsenic in soil of West Bengal was reported to be as high as 19.4 mg kg -1 Page 102

5 (Roychowdhury et al. 2005). So, the 20.0 mg kg -1 arsenic dosing in pot soil has become very important. The arsenic content of the paddy field soil of West Bengal was reported to be significantly correlated with the arsenic content of the irrigation water (r= 0.522) (Bhattacharya et al. 2010b), thus there is a high possibility of increase of arsenic concentration in the paddy field soil of the whole arsenic affected areas of West Bengal in near future. In that scenario consumption of rice, staple food of this region will be another potent route for entrance of arsenic toxicity in the human food chain along with the present drinking water pathway. Table 1: Effect of soil arsenic concentrations on arsenic contents of four widely cultivated rice (Oryza sativa L.) varieties of West Bengal, India Rice varieties Arsenic treatment (mg kg -1 soil) Concentrations of arsenic (mean ± SD) in various parts of the rice plant (mg kg -1 dry weight) Root Straw Husk Grain Control Tulsa 5.20 ± ± 0.07 BDL BDL Ratna 3.03 ± ± ± ± 0.01 IR ± ± ± ± 0.00 Gangakaveri 6.74 ± ± ± 0.01 BDL 5.0 Tulsa ± ± ± ± 0.02 Ratna 8.78 ± ± ± ± 0.02 IR ± ± ± ± 0.01 Gangakaveri ± ± ± ± Tulsa ± ± ± ± 0.02 Ratna ± ± ± ± 0.03 IR ± ± ± ± 0.05 Gangakaveri ± ± ± ± Tulsa ± ± ± ± 0.03 Ratna ± ± ± ± 0.10 IR ± ± ± ± 0.05 Gangakaveri ± ± ± ± Tulsa ± ± ± ± 0.04 Ratna ± ± ± ± 0.11 IR ± ± ± ± 0.06 Gangakaveri ± ± ± ± Tulsa ± ± ± ± 0.08 Ratna ± ± ± ± 0.16 IR ± ± ± ± 0.09 Gangakaveri ± ± ± ± 0.18 BDL: Below the detection limit (< mg kg -1 ) Irrespective of the rice variety arsenic accumulated mostly in the root of the rice plant. For an example at 10.0 mg kg -1 arsenic dosing in pot soil the accumulation of arsenic in the root was in the range ± ± 2.44 mg kg -1 dry weights. It was followed by the accumulation in the straw (1.34 ± 0.25 Page 103

6 2.41 ± 0.14 mg kg -1 dry weight of arsenic), husk (0.51 ± ± 0.07 mg kg -1 dry weight of arsenic) and grain (0.41 ± ± 0.03 mg kg -1 dry weight of arsenic) parts of the rice plant. This trend of accumulation of arsenic (root>straw>husk>grain) is in good agreement with the previous findings by Abedin et al. (2002), Rahman et al. (2007) and Bhattacharya et al. (2010a). Rahman et al. (2007) reported that regardless of rice varieties, accumulation of arsenic were 28 and 75 folds higher in the root than that of the shoot and the raw rice grain, respectively. Although the actual mechanism of higher accumulation of arsenic in the rice root is still not well understood, Liu et al. (2004) reported that the iron oxides (iron plaques) formed around the root of the rice plant bind the arsenic and reduce its translocation to the above ground tissues (straw, husk and grain) of the plant. 4. Conclusions The potential of arsenic contamination is increasing day by day in the groundwater of West Bengal, India and enhancing the human health risk from arsenic toxicity via water-soil-plant system. Thus prompt management strategy should be taken by the Government in encouraging cultivation of less arsenic accumulated rice varieties like Tulsa in arsenic-contaminated areas of West Bengal. Along with it, rice varieties which require huge irrigation water and which are found to accumulate higher amount of arsenic, viz. IR 50 and Gangakaveri are to be avoided. More emphasis should be given for cultivation of crops accumulating very low amount of arsenic like, wheat, garlic, lentil, beans, green chili, tomato, bitter gourd, lady s finger, lemon and turmeric. This will support the economy of the poor people and also reduce the potential entry of arsenic in human food chain. Acknowledgements The authors are thankful to the Department of Environment, Government of West Bengal, India for providing fund to carry out the investigation and to the Department of Environmental Science, University of Kalyani, West Bengal, India for providing the laboratory facilities. Page 104

7 References: Abedin MJ, Feldmann J, Meharg AA (2002) Uptake kinetics of arsenic species in rice plants. Plant Physiol 128: Alam MGM, Snow ET, Tanaka A (2003) Arsenic and heavy metal contamination of vegetables grown in Samta village, Bangladesh. Sci Total Environ 308:83 96 Bhattacharya P, Samal AC, Majumdar J, Santra SC (2010a) Accumulation of arsenic and its distribution in rice plant (Oryza sativa L.) in Gangetic West Bengal, India. Paddy Water Environ 8(1):63-70 Bhattacharya P, Samal AC, Majumdar J, Santra SC (2010b) Arsenic contamination in rice, wheat, pulses and vegetables: A study in an arsenic affected area of West Bengal, India. Water Air Soil Pollut 213:3-13 Dahal BM, Fuerhacker M, Mentler A, Karki KB, Shrestha RR, Blum WEH (2008) Arsenic contamination of soils and agricultural plants through irrigation water in Nepal. Environ Pollut 155: Das HK, Sengupta PK, Hossain A, Islam M, Islam F (2002) Diversity of environmental arsenic pollution in Bangladesh. In: Ahmed MF, Tanveer SA, Badruzzaman ABM (eds) Bangladesh environment, vol. 1. Dhaka, Bangladesh: Bangladesh Paribesh Andolon, p Duxbury JM, Mayer AB, Lauren JG, Hassan N (2003) Food chain aspects of arsenic contamination in Bangladesh: Effects on quality and productivity of rice. J Environ Sci Heal A 38: 1 69 Guha-Mazumder DN, Haque R, Ghose N, De BK, Santra A, Chakraborty D (2000) Arsenic in drinking water and the prevalence of respiratory effects in West Bengal, India. Int J Epidemiol 29: Lehoczky E, Ne meth T, Kiss Z, Szalai T (2002) Heavy metal uptake by ryegrass, lettuce and white mustard plants on different soils. In: 17th WCSS, August, Thailand. Symp. No. 60, Paper No Liu WJ, Zhu YG, Smith A, Smith SE (2004) Do iron plaque and genotypes affect arsenate uptake and translocation by rice seedlings (Oryza sativa L.) grown in solution culture. J Exp Bot 55(403): Meharg AA, Williams PN, Adomako E, Lawgali YY, Deacon C, Villada A, Sun G, Zhu YG, Feldmann J, Raab A, Zhao FJ, Islam R, Hossain S, Yanai J (2009) Geographical variation in total and inorganic arsenic content of polished (white) rice. Environ Sci Technol 43(5): Norra S, Berner ZA, Agarwala P, Wagner F, Chandrasekharam D, Stüben D (2005) Impact of irrigation with arsenic rich groundwater on soil and crops: a geochemical case study in West Bengal delta plain, India. Appl Geochem 20: Rahman M (2002) Arsenic and contamination of drinking-water in Bangladesh: a public-health perspective. J Health Popul Nutr 20: Rahman MA, Hasegawa H, Rahman MM, Rahman MA, Miah MAM (2007) Accumulation of arsenic in tissues of rice plant (Oryza sativa L.) and its distribution in fractions of rice grain. Chemosphere 69: Rahman MA, Hasegawa H, Rahman MM, Miah MAM, Tasmin A (2008) Arsenic accumulation in rice (Oryza sativa L.): Human exposure through food chain. Ecotox Environ Safe 69: Roberts LC, Hug SJ, Dittmar J, Voegelin A, Kretzschmar R, Wehrli B, Cirpka OA, Saha GC, Ali MA, Badruzzaman ABM (2010) Arsenic release from paddy soils during monsoon flooding. Nat Geosci 3:53-59 Roychowdhury T, Tokunaga H, Uchino T, Ando M (2005) Effect of arsenic-contaminated irrigation water on agricultural land, soil and plants in West Bengal, India. Chemosphere 58: Samal AC, Bhattacharya Piyal, Santra SC, Kar S (2010) Transfer of arsenic from contaminated groundwater and soils to crops and vegetables: A study in Gangetic delta of West Bengal, India. In: Bundschuh J, Bhattacharya P (eds) Arsenic in geosphere and human diseases. Taylor and Francis, London, p Srivastava AK, Hasan SK, Srivastava RC (2001) Arsenicism in India: dermal lesions and hair levels. Arch Environ Health 56:562 Welsch EP, Crock JG, Sanzolone R (1990) Trace level determination of arsenic and selenium using continuous flow hydride generation atomic absorption spectrophotometry (HG-AAS). In: Arbogast BF (ed) Quality assurance manual for the branch of geochemistry. Open-File Rep US Geological Survey, Reston,VA. p Page 105

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Available online at www.pelagiaresearchlibrary.com Advances in Applied Science Research, 2016, 7(4):168-175 ISSN: 0976-8610 CODEN (USA): AASRFC Arsenic toxicity through contaminated selected blocks of