Scientia Horticulturae 113 (2007) 250254 www.elsevier.

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Translocation of heavy metals to tomato (Solanum lycopersicom L.) fruit irrigated with treated wastewater
O. Al-Lahham a,1, N.M. El Assi b,*, M. Fayyad c
b a The Royal Scientic Society, Amman, Jordan Department of Horticulture and Field Crops, College of Agriculture, University of Jordan, P.O. Box 13367, Amman 11942, Jordan c Water and Environment Research and Study Center, University of Jordan, Jordan

Received 1 January 2007; received in revised form 18 March 2007; accepted 22 March 2007

Abstract A eld experiment was conducted to investigate the extent of translocation of heavy metals to tomato (Solanum lycopersicom L. cvs. GS12 and RS589956) fruit produced in an open eld near to Abu-Nusiar Wastewater Treatment Plant, Amman-Jordan. Seedlings were planted during the seasons of 1999 and 2000 and furrow irrigated with different mixtures of potable water to treated wastewater {100%:0% (1:0, control); 25%:75% (1:3); 50%:50% (1:1); 0%:100% (0:1)}. Tomato fruit, soil and water were examine for heavy metals concentrations, and changes in the pH and electrical conductivity (EC) of the soil were tested. The obtained results revealed an increase in the concentrations of Cu, Mn and Fe, in the soil correlated with high concentrations found in the wastewater. Additionally, an increase in the pH and EC in the soil was observed with increasing the proportions of wastewater. Results of tomato fruit analysis showed an increased concentration of Fe, Cu, Ni, Mn and Zn in the cultivar RS589956, whereas, an increased concentration of Mn and Zn were detected in the cultivar GS12, but no accumulation of Cd and Pb in both cultivars. The accumulation of heavy metals in fruit was below the Jordanian standard limits, thus, the use of treated wastewater in irrigation might be feasible. # 2007 Elsevier B.V. All rights reserved.
Keywords: Heavy metals; Irrigation; Potable water; Solanum lycopersicom; Wastewater

1. Introduction Treated efuent can be used for irrigation under controlled conditions that minimize health risks from pathogenic and toxic pollution to the agricultural products, soils, surface and ground water (Mahasneh et al., 1989a). Moreover, treated wastewater is a good source of water to control problems such as wastewater disposition, lack of water availability in arid zones, in addition, it can improve soil quality for crop production (Jimenez-Cisneros, 1995). Wastewater and sewage efuents contain signicant quantities of heavy metals and other substances that may be toxic to people but benecial to horticultural crops (Butler et al., 1964; Sanderson, 1986) Metals such as Zn, Cd, Pb, Fe, Cu, Mn and Mo may be phytotoxic and/or if accumulated in the fruit will impose

* Corresponding author. Tel.: +962 6 5355000x22346; fax: +962 6 5355577. E-mail addresses: najibasi@ju.edu.jo (N.M. El Assi), water1@ju.edu.jo (M. Fayyad). 1 Tel.: +962 6 5344701. 0304-4238/$ see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2007.03.017

a health risk to humans (Omran et al., 1988). Human health risks, such as parasitic infections and transfer of heavy metals in the food chain, represent the main limitations which led many countries to issue more rigid regulations with respect to pathogenic and heavy metal contents in wastewater and sludge reused in agriculture, as well as to establish maximum permissible limits for heavy metals in soil (Siebe, 1995). Kirkham (1986), however, suggested that heavy metals in wastewater used on vegetables are unlikely to cause adverse effects. Efforts to explore such possibilities, in a semi-arid country such as Jordan, must take place to offer safe alternatives to maintain sufcient crop production with high quality for the increasing population. The objective of this research was to investigate the extent of translocation of heavy metals to the fruit following irrigation with treated wastewater. Heavy metals concentration in treated wastewater, soil and tomato fruit were measured and compared to several standards limits. Additionally, the impact of treated wastewater on the soil pH and electrical conductivity were determined.

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2. Material and methods 2.1. Field experiment In 2 consecutive years, 1999 and 2000, tomato seedlings of two cultivars, GS12 and RS589956, were transplanted, with no fertilizers added, in an open eld near to Abu-Nusair Wastewater Treatment Plant, Amman-Jordan. Four treatments were applied in a three replicates, randomized complete block design (RCBD) with split plot arrangements. Three blocks, each consisted of two plots 11 m 5.5 m each containing one cultivar. Experimental treatments were two cultivars grown with four mixtures, applied by furrow irrigation, of potable water to treated wastewater ratios at the following proportions: 0%:100% (0:1); 25%:75% (1:3); 50%:50% (1:1); 100%:0% (1:0) (control). Irrigation needs of the plants were monitored by a ceramic cup Tensiometer that was installed prior to planting at 25 cm below the soil surface in one of the plots of each block. A 67 mm of water per rrigation to bring the Tensiometer reading to 0.3 bar at 0.25 m soil depth was delivered twice a week to meet the crop needs of irrigation (Klue et al., 1986; AlNakshabandi et al., 1997). Abu-Nusair Waste Water Treatment Plant is an activated sludge-extended aeration plant comprises of a mechanical screen, grit removal tanks, primary sedimentation tanks, extended aeration tanks, nal sedimentation tanks and nally chlorination tanks. 2.2. Sample collection and preparation Tomato fruit samples were hand harvested at an advanced full red stage of maturity (vine-ripe) by the end of July till the end of September at weekly intervals between harvests. Twenty fruits 6 plots 4 weeks 2 seasons = 960 fruits were tested in this experiment. Harvested fruits were transported immediately to the Horticultural Laboratory at the Faculty of Agriculture, University of Jordan for laboratory analysis.
Table 1 Heavy metal standards of drinking watera,b,c (mg/l), treated wastewaterd (mg/l), tomato juicee (mg/kg), processed tomato concentratesf (mg/kg) and tomato ketchupg (mg/kg) Standard Heavy metals Cd EU U.S.b JS 286c JS 893d JS 283e JS 41f; 355g
a b c d e f g a

Soil samples (four samples from each depth) were taken randomly at three depths (020, 2040 and 4060 cm) in each block, prior to planting and after the last harvest, by using an Auger. The soil collected from each depth was mixed, dried in a green house for 2 days, crushed and sieved with a 2 mm sieve. Samples were tested for their pH, electrical conductivity and heavy metals (Klue et al., 1986). The concentration of heavy metals was determined by the Diethylenetriaminpentaacetic acid (DTPA) method. The preparation and extracting procedures were carried out according to Page et al. (1982). Ten grams of air-dried soil were weighed, and 20 ml of DTPA extracting solution adjusted to 7.3 pH were added, and mixture was shaken at 120 cycles/min speed for 2 h, nally ltered through Whatman No. 42 lter paper. Water samples were collected in polypropylene bottles. After ltration, samples were preserved by adding 1.5 ml concentrated nitric acid (HNO3) to reach pH < 2, and stored in a refrigerator at about 4 8C to prevent any possible change in volume due to evaporation. Potable water samples, were analyzed directly without digestion, whereas, treated wastewater samples were concentrated from 250 to 50 ml each using a Rotary Evaporator, and then ltered. 2.3. Measurements The pH of the soil was measured after adding 5 ml of distilled water to 5 g of air-dried soil, and mixing thoroughly for 5 s using a magnetic stirrer. The pH of the was determined using a pH meter (inolab pH level 1, Wissenschalich Technishe Werkstaffen, Germany). The electrical conductivity of the soil was determined directly by using a Conductivity Meter (JENWAY 3420, Electrochemistry Analyzer, UK) before planting and after the last harvest (Klue et al., 1986). Heavy metals studied in this research were the dissolved metals {dened as those constituents (metals) of an unacidied sample that pass through a 0.45 mm membrane lter (American Public Health Association, 1998)}. The metals [cadmium (Cd), copper (Cu), iron (Fe), manganese (Mn), nickel (Ni), lead (Pb) and zinc (Zn)] in the soil (OzoresHampton et al., 1994), in water (American Public Health Association, 1998) and in fruit were determined by Graphite Furnace Atomic Absorption Spectrophotometry (PEE UNICAM 9090, PHILIPS, UK). Heavy metals results are reported and discussed in light of some standards prescribed by several institutions (Purdom, 1980; Institution for Standards and Metrology 1995, 1996, 1997 a and b, 2001) in Table 1. 3. Statistical analysis Representative results from the 2-year experiment are reported. A completely randomized block design (CRBD) was used in these experiments. Analyses of variance (ANOVA) were performed using the Statistical Analysis Systems Computer Package (SAS Institute, 1996). Treatment means were compared by the least signicant difference test at P = 0.05.

Cu 0.05 1.00 1.01.5 0.20 5.00 10.0

Fe 0.10 0.30 0.10.5 5.00 15.0

Mn 0.05 0.05 0.10 0.20

Zn 5.00 5.00 3.00 2.00 5.00 1.50

Ni 0.01 0.20

Pb 0.10 0.05 0.02 5.00 0.30

0.01 0.01 0.03 0.01

From Purdom (1980) (Source: World Health Organization, 1970). From Purdom (1980) (Source: U.S. Public Health Service, 1962). ISM (1997a,b). ISM (1995). ISM (2001, second ed.). ISM (1997a,b). ISM (1996).

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O. Al-Lahham et al. / Scientia Horticulturae 113 (2007) 250254 Table 3 Heavy metal concentrations in four treatments (control 1:0; 1:1; 1:3 and 0:1 potable water to treated wastewater) Treatment Heavy metals a Cd 1:0 (control) 1:1 1:3 0:1 Signicance LSD
a *

4. Results and discussion Slight increases in the soil pH values were observed after the last harvest as compared to the values obtained before planting with signicant differences (Table 2). This is in agreement with similar results obtained by Purdom (1980) and Shatanawi (1994) who proposed that the use of treated wastewater to irrigate crops can increase the soil pH. An increase in the soil pH was observed with increasing soil depth, mainly after harvest (Table 2), conrming similar results obtained earlier by Shatanawi (1994). However, such an increase in soil pH had no effect on tomato fruit pH that was always within the range of 4 (Al-Lahham et al., 2003), which is typical of tomato fruit pH (Balibrea et al., 1997). Soil EC increased from 1418 to 1431 ms cm prior to planting to 1710 and to 1676 ms cm after harvest in the 020 and 40 60 cm soil depths, respectively (Table 2). Similar results were reported by Shatanawi (1994), whereas, Khatari and Jamjom (1988) and Fardous and Jamjoum (1996) found an increase only in the soil EC at the surface of the soil. They suggested that the use of treated wastewater in irrigation might be the reason for the increase in soil EC. Furthermore, the increase in EC observed in our work can also be explained by reports from Kirkham (1986), who suggested that salt concentrations in domestic wastewater vary widely according to the salinity of the local water source, and by the ndings of Maurer et al. (1995), who mentioned that, the greatest disadvantages of reclaimed wastewater was the high salinity. A decline, however, in soil EC at the 2040 cm soil depth from 1304 to 1064 ms cm was observed (Table 2), similarly Al-Nakshabandi et al. (1997), concluded that the leaching and displacement of salt by irrigation was the most probable reason for such decline. The results of heavy metals analysis of the soil showed that, after irrigation with treated wastewater, there was no accumulation of Cd and Pb in the soil, while, the content of Zn and Ni remained stable (Table 2). The Cu, Fe and Mn concentrations measured after harvest increased at same soil depths as compared to concentrations measured prior to planting (Table 2). Such results can be attributed to the presence of these different metals in the treated wastewater that might

Cu 0.330 0.670 0.970 1.360

*

Fe 4.130 11.980 12.220 12.220

*

Mn 0.180 0.160 0.260 0.370 ns

Zn 2.460 3.970 10.150 11.790

*

Ni 0.300 0.550 0.760 0.210

*

Pb 0.000 0.000 0.000 0.000 ns

0.000 0.000 0.000 0.000 ns

0.199

2.778

2.828

0.509

Means are the average of six samples. Signicant at P 0.05.

have accumulated at different soil depths after irrigation (Shatanawi, 1994). For heavy metal analysis, treated wastewater and potable water were sampled twice a month from July to September. Heavy metal concentration in the irrigation treatment with different concentrations of treated wastewater and potable water are shown in Table 3. No detectable concentrations of Cd or Pb were found in all treatments. Additionally, no signicant differences were found for Mn concentration in all treatments. Table 3 reveals that the concentrations of Fe, Cu, Ni and Zn were signicantly different among treatments with the highest value obtained for wastewater (0:1), and the lowest was for the control (1:0). Similar results were also obtained by Kirkham (1986), who stated that, concentrations of heavy elements in treated wastewater are higher than the limits established for drinking water. Additionally, Omran et al. (1988) concluded that, potential disadvantages of using reclaimed wastewater include the accumulation of phytotoxic levels of heavy metals. In the present study the concentration of heavy metals (except Cd and Pb) in treated wastewater (Table 3) were higher than the limits prescribed by Jordan standards for treated domestic wastewater (Table 1). This could be related to the efuent source that might have contained a large amount of these substances, with the exception of Cd and Pb, since it was from domestic origin with no industrial waste contamination.

Table 2 Values of the soil pH, electrical conductivity (ms cm) and heavy metals concentrations (mg/kg) at three depths (020, 2040 and 4060 cm) in the soil measured prior to planting and after the last harvest following irrigation with treated wastewater Testa Prior to planting 020 pH EC Cd Cu Fe Mn Zn Ni Pb
a *

After harvest 040 7.18 1604 0.015 0.979 5.076 3.665 10.370 0.350 0.051 4060 7.32 1431 0.000 0.670 5.426 4.398 11.270 0.270 0.015 020 7.60 1710 0.003 0.82 3.903 3.920 8.920 0.287 0.041 2040 7.60 1064 0.018 1.440 5.393 3.904 10.770 0.231 0.030 4060 8.20 1676 0.002 0.725 5.942 4.431 11.650 0.297 0.000

Signicance

LSD

7.46 1418 0.003 0.595 3.731 3.801 8.112 0.280 0.034

* * * * * * * * *

0.2182 57.57 0.003 0.090 0.437 0.171 0.744 0.024 0.173

Means are the average of 12 samples. Signicant at P 0.05.

O. Al-Lahham et al. / Scientia Horticulturae 113 (2007) 250254 Table 4 Heavy metal concentration in the treated wastewater for 3 months Month Heavy metalsa Cd July August September Signicance LSD
a *

253

Table 5 Heavy metal accumulation in the fruit following four irrigation treatments (control 1:0; 1:1; 1:3 and 0:1 potable water to treated wastewater) Pb 0.000 0.000 0.000 ns Treatment Heavy metals a Cd GS12 1:0 (control) 1:1 1:3 0:1 RS589956 1:0 (control) 1:1 1:3 0:1
a

Cu 1.137 0.440 0.910

*

Fe 11.700 8.190 10.530

*

Mn 0.240 0.270 0.220 ns

Zn 7.230 5.420 8.620

*

Ni 0.680 0.100 1.340

*

0.000 0.000 0.000 ns

Cu 0.000 0.000 0.000 0.000 0.000 0.025 0.050 0.075

Fe 0.000 0.000 0.000 0.000 0.000 0.007 0.020 0.035

Mn 0.000 0.000 0.013 0.025 0.000 0.000 0.000 0.013

Zn 0.000 0.000 0.000 0.025 0.000 0.000 0.050 0.100

Ni 0.000 0.000 0.000 0.000 0.000 0.100 0.100 0.300

Pb 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

0.730

2.406

2.449

0.441

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

Means are the average of six samples. Signicant at P 0.05.

Purdom (1980), reported that, wastewater sources differ according to the water usage and region. Since about 7% of domestic water is consumed, thus, about 93% must eventually become wastewater. The pollutants in domestic wastewater arise from food preparation, household and body cleansing functions, body excretions and industrial operations. The concentrations of Fe, Mn and Ni in potable water treatment, shown in Table 3, were higher than the limits prescribed by Jordan standards for drinking water, United States Public Health Service for drinking water and European drinking water standards (Table 1). Table 4 shows the concentrations of Fe, Cu, Ni and Zn in the treated wastewater over 3 months. In July, Fe and Cu had the highest concentration compared with those of August and September (Table 4). Furthermore, in September, Ni and Zn had the highest concentration compared with those of July and August (Table 4). Concentrations of Mn did not show signicant differences between months, whereas, Cd and Pb were not detectable in the 3 months (Table 4). Table 5 shows the content of heavy metals in two tomato cultivars (GS12, RS589956) irrigated with different concentrations of treated wastewater. The results indicate that, there was no accumulation of Cd and Pb in both cultivars (Table 5). This might be due mainly to the absence of Cd and Pb in both irrigation water and soil. Additionally, in GS12vcultivar, a negligible accumulation of Mn, and Zn (Table 5), that was below the Jordanian standards (Table 1). The highest concentration for Mn and Zn was obtained for the 0:1 treated wastewater irrigation treatment, which was also lower than Jordanian standard limits (Table 1). The accumulation of heavy metals was more evident in the RS589956 cultivar as compared to GS12 cultivar (Table 5),, however, the accumulated Fe and Mn were below the Jordanian standards for tomato juice, and for processed tomato (Table 1). Ni was detected in all treatments but control and increasing with enrichment in wastewater. The concentration of Zn was below the Jordanian standards for tomato juice (Table 1). The element Zn had the highest concentration in the 0:1 treatment, and was still detectable in the 1:3 treatment but not in others (Table 5). Cu had a small accumulation in fruit, but was detected in all treatments with wastewater and had the highest concentration in fruits from the 0:1 treatment, but was still below the Jordanian standards for tomato juice (Table 1). No accumula-

Means are the average of 60 fruits.

tion of heavy metals was detected in the fruit from both cultivars irrigated with potable water (Table 5). These results indicate that, the accumulation of heavy metals varied according to cultivar, but was more pronounced with increasing the proportions treated wastewater used in irrigation of the plants (the pattern of accumulation follows the order of 1:0 < 1:1 < 1:3 < 0:1). Similarly, Shatanawi (1994) found that, heavy metals increased in eggplant fruit and leaves by using treated wastewater irrigation as compared with fresh water, which conrms the ndings that the treated wastewater was also a factor in determining the heavy metal accumulation. In the two cultivars irrigated with potable water (control), no accumulation of heavy metals in the fruit was noticed. Berry et al. (1980) found that, heavy metals taken up by vegetables grown with wastewater tend to remain elements in the roots, and only a fraction of the heavy elements absorbed is translocated to the tops, part of which reaches the fruit. Fazeli et al. (1991), provided evidence that the accumulation of heavy metals in different parts of the plant body might be due to the tendency of different parts of the plant to accumulate certain amounts of metals. Ardakani et al. (1988) reported that, plant species and plant parts inuence the uptake and accumulation of heavy metals by plants. This conrms the results obtained in this experiment that the two tomato cultivars and the different fruit parts actually differ in their ability to accumulate heavy metals. 5. Conclusions Irrigation with treated efuent increased the concentration of Cu, Fe and Mn accumulation at different soil depths, with an increase in soil pH and salinity. The increased levels of these heavy metals in the soil was analogous to the increased concentration of these metals in the treated wastewater, indicating repositioning into soil, and then a strong possibility of, at least, partial translocation into the fruit. The accumulation of heavy metals in tomato irrigated with treated wastewater was affected according to cultivar, plant part and the use of treated wastewater. Tomato fruit from the GS12 cultivar accumulated Mn and Zn, whereas, fruit from RS589956 cultivar

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O. Al-Lahham et al. / Scientia Horticulturae 113 (2007) 250254 Institution for Standards and Metrology, 1997a. Jordan Standard for Water Drinking Water. JS 286:1997. Amman, Jordan. Institution for Standards and Metrology, 1997b. Jordan Standard for Vegetable ProductsProcessed Tomato Concentrates. JS 41:1997. Amman, Jordan. Institution for Standards and Metrology, 2001. Jordan Standard for Drinks and JuicesTomato Juice Preserved Exclusively by Physical Means, second ed. JS 283:2001. Amman, Jordan. Jimenez-Cisneros, B., 1995. Wastewater reuse to increase soil productivity. J. Water Sci. Technol. 32 (12), 173180. Khatari, S., Jamjom, K., 1988. The effect of treated wastewater on the concentration of nutrients and some heavy metals in different parts of corn plant and some chemical soil properties. Dirasat 15 (11), 2944. Kirkham, M.B., 1986. Problems of using wastewater on vegetable crops. HortScience 21 (1), 2427. Klue, A., Campbell, G.S., Nielsen, D.R., Jackson, R.D., Mortland, M.M., Klute, A., 1986. Methods of Soil Analysis. Part I. Physical and Mineralogical Methods, second ed. American Society of Agronomy Inc. Soil. Mahasneh, A., Al-Wir, A., Salameh, E., Batarseh, L., Shatanawi, M., Rimawi, O., Judeh, O., Khattari, S., Oweis, T., 1989a. Treated Wastewater Reuse in Agriculture. Part I. Hussein Medical Center Project, No. 12. Bulletin of Water Research and Study Center. University of Jordan. Maurer, M.A., Davies, F.S., Graetz, D.A., 1995. Reclaimed wastewater irrigation and fertilization of mature Redblush grapefruit trees on spodosols in Florida. J. Am. Soc. Hort. Sci. 120 (3), 394402. Omran, M.S., Waly, T.M., Abd Elnaim, E.M., El Nashar, B.M.B, 1988. Effect of sewage irrigation on yield tree components and heavy metals accumulation in Navel orange trees. Boil. Wastes 23, 1724. Ozores-Hampton, M., Schaffer, B., Bryan, H.H., 1994. Nutrient concentrations, growth and yield of tomato and squash in municipal solid-waste-amended soil. Hort. Sci. 29 (7), 785788. Page, A.L., Miller, R.H., Keeny, D.R., 1982. Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties, second ed. American Society of Agronomy, Soil Science Society of America, Madison, WI, USA. Purdom, P.W., 1980. Environmental Health, second ed. Academic Press Inc., (London) Ltd., UK. Sanderson, K.C., 1986. Introduction to the workshop on wastewater utilization in horticulture. Hort. Sci. 21, 2324. SAS Institute, 1996. Statistical Analysis Systems Computer Package. SAS Institute, Cary, NC, USA. Shatanawi, M., 1994. Minimizing environmental problems associated with the use of treated wastewater for irrigation in Jordan valleyphase I. Technical Report No. 18. Water and Environmental Research and Study Center, University of Jordan. Amman, Jordan. Siebe, C., 1995. Heavy metal availability to plants in soils irrigated with wastewater from Mexico city. J. Water Sci. Technol. 32 (12), 2934.

accumulated Fe, Cu, Ni, Mn and Zn. Thus, it is believed that, partial translocation of heavy metals from the soil to the fruit occurred, due to the presence of these metals in treated efuent, however, the concentration of these heavy metals in fruit were below the standard limits. Therefore, the use of wastewater in irrigation of tomato fruit might be feasible because of its high nutritive value that may improve plant growth, reduce fertilizer application rates and increase productivity of poor soils. References
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