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The effect of bullet removal and vegetation on mobility of Pb in shooting range soils
Chemosphere 160 (2016) 252e257
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The effect of bullet removal and vegetation on mobility of Pb in shooting range soils Abioye O. Fayiga a, *, Uttam Saha a, b a b
Soil and Water Science Department, University of Florida, Gainesville, FL 32611-0290, USA University of Georgia Cooperative Extension, 2300 College Station Road, Athens, GA 30602, USA
h i g h l i g h t s
g r a p h i c a l a b s t r a c t
Two best management practices for shooting ranges, bullet removal and vegetation, were evaluated in a green house study. Bullet removal reduced total soil Pb and increased DOC in leachates. Bullet removal increased bioavailable Pb in un-vegetated soils. Vegetation reduced leaching of Pb in two shooting range soils. St. Augustine grass accumulated up to 5021 mg Pb/kg in roots.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 March 2016 Received in revised form 19 June 2016 Accepted 26 June 2016 Available online 6 July 2016
Lead (Pb) contamination at shooting ranges is a public health concern because Pb is a toxic metal. An experiment was conducted to determine the effect of two best management practices; bullet removal and vegetation, on bioavailability and leachability of Pb in three shooting range (SR) soils. St. Augustine grass was grown in sieved (2 mm) and un-sieved SR soils for 8 weeks after which leachates, soil and plant samples were analyzed. Bullet removal reduced total soil Pb, increased Mehlich-3 Pb in unvegetated soils and increased dissolved organic carbon (DOC) in all soils. Bullet removal increased leaching in two SR soils while grasses reduced leaching but increased water soluble Pb in two SR soils. The roots of the grasses were able to accumulate more Pb in the root (1893e5021 mg kg1) than the aboveground biomass (252e880 mg kg1) due to mobilization of Pb in the rhizosphere. Grasses had a higher plant biomass in unsieved soils suggesting tolerance to the presence of bullets in the unsieved soils. Results suggest that bullet removal probably increased microbial activity and Pb bioavailability in the soil. The leaching and bioavailability of Pb in shooting range soils depends on biological activities and chemical processes in the soil. © 2016 Elsevier Ltd. All rights reserved.
Handling Editor: Martine Leermakers Keywords: Shooting ranges Pb St. Augustine grass Dissolved organic carbon Rhizosphere Mehlich-3 Pb
1. Introduction Soil contamination with lead (Pb) has been reported in shooting ranges (SR) worldwide (Dermatas et al., 2006; Siebielec and
* Corresponding author. E-mail address: [email protected] (A.O. Fayiga). http://dx.doi.org/10.1016/j.chemosphere.2016.06.098 0045-6535/© 2016 Elsevier Ltd. All rights reserved.
Chaney, 2012; Sanderson et al., 2014). Approximately 80,000 tons/year of Pb was used in the production of bullets and shot in the United States in the late 1990s (USEPA, 2005; Hardison et al., 2004). Bullets are fragmented and pulverized upon impact with ground, backstop, berms or bullet trap at SR (O’Connor et al., 2009). It has been reported that soil and Pb metallic fragment particle sizes play a dominant role in the rate and amount of Pb release in SR soils
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(Dermatas et al., 2006). Weathering of fragmented Pb bullets eventually results in elevated total Pb concentrations in SR soils especially those that have been in operation for a long period of time. Some of the best management practices (BMP) used to mitigate Pb contamination in SR includes sieving to remove the bullet fragments and vegetation to provide a cover for the soil (USEPA, 2005). Removal of used bullets from contaminated SR soils is expected to reduce Pb contamination at these sites. However, previous studies have reported that the abrasive action of mechanical sieving transferred metallic Pb to the soil fraction (<2 mm) and increased total Pb in the soil (Yin et al., 2010; Liu et al., 2013). It is imperative to evaluate the effect of bullet removal on Pb bioavailability since total concentrations do not provide adequate information on toxicity of heavy metals to the users and biota at these sites. The total amount of metals in the soil is not available because they are adsorbed or bound by organic and inorganic solid phases in the soil such as organic matter, Fe and Al oxides and clay minerals (Fayiga and Saha, 2016). Since bioavailability is the portion that is available or can be absorbed by living organisms, it is a better estimate of environmental risk and toxicity (McLaughlin, 2001; Hettiarachchi and Pierzynski, 2004). The speciation of Pb is also important because it’s the key to understanding the fate and bioavailability of Pb in the environment (Beak et al., 2006). Water-soluble concentration has also been said to be the most eco-toxicologically relevant fraction in the environment due to its high contamination potential of the surface and ground water through leaching and runoff (Meers et al., 2006; Levei et al., 2010). It may also control plant uptake in vegetated soils. The presence of vegetation in SR is significant because some plants are tolerant to metals and can immobilize contaminants in the root zone (Cao et al., 2003a). The metal tolerant plants can be used for revegetation of contaminated sites (Shu et al., 2002). Butler et al. (2010) reported that vegetation alone reduced metal concentrations in run-off water by about nine times compared to the control. The combination of vegetation (Houben et al., 2012) and bullet removal in SR may be a cost efficient and sustainable method of remediation for contaminated SR soils. Therefore, the objectives of this study were to determine the effect of bullet removal and vegetation on Pb leachability and bioavailability in SR soils. 2. Materials and method 2.1. Experimental set up The soils used in this experiment were collected from the berms of three rifle shooting ranges (SR1, SR2 and SR3) in Florida. SR1 has been in operation for 6 years whereas the SR2 and SR3 have been in operation for 15 and 30 years respectively. We took random samples from top, bottom and middle of the berms and mixed them up to make a representative 100 kg composite sample. The soils were hand mixed and air-dried for a week, with 50 kg passed through a 2-mm sieve (no bullets), while the other 50 kg was not sieved (with bullets). Shooting range soil weighing 1.6 kg was thoroughly hand mixed with 2 g of slow release fertilizer (18-9-18, N-P2O5-K2O) and placed in a plastic pot with a diameter of 0.14 m and height 0.16 m (2.5 L). One plug of St. Augustine grass (Stenotaphrum secundatum) was planted in pots containing sieved or un-sieved soil, with soil alone as controls with four replications. The plants were grown in the University of Florida greenhouse where the average temperature ranged from 14 (night) to 30 C (day), with an average photosynthetic photon flux density of 825 mmol m2 s1. The plants were watered with deionized water and a petri dish was placed under
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each pot to collect potential leachates during the experiment. Leachate was collected every two weeks and analyzed for pH, DOC and Pb content. The grasses were harvested after 8 weeks and separated into aboveground and belowground biomass (roots). Fresh plant samples were rinsed with deionized water, dried in the oven for 3 days at 65 C and then ground in a mill. The weights of fresh and dry biomass of grass in each pot were determined. Soil samples were collected after harvesting and analyzed for pH, water-soluble Pb, Mehlich-3-Pb and total Pb. Rhizosphere soil collected from the roots was separated from the bulk soil and analyzed for water-soluble Pb and soil pH. Unsieved soils were sieved after harvest and bullet mass determined.
2.2. Chemical analysis Characterization of sieved soils were done before the experiment by routinely analyzing for CEC, organic matter, particle size distribution, soil pH and water soluble Pb. Detailed methods of analysis can be found in a previous publication (Fayiga et al., 2011). Non-crystalline aluminum and iron in the soils were extracted by shaking 2 g soil in 10 ml acid ammonium oxalate for 4 h in the dark (McKeague and Day, 1966). Fe and Al in the extract were measured by using a flame atomic absorption spectrophotometer (FAAS, Varian 220 FS with SIPS, Walnut Creek, CA). Results are presented in Table 1. Soil and plant samples from experiment were digested with nitric acid and hydrogen peroxide using the Hot Block Digestion System (Environmental Express, Mt. Pleasant, SC; EPA Method 3050a). Total Pb contents of soil/plant digest; filtrate/extracts and leachates were analyzed on FAAS. Dissolved organic carbon in leachates from soils was analyzed using a total organic carbon analyzer (TOC-5050 A, Shimadzu Corporation, Japan) which was calibrated with standards. Watersoluble Pb was determined in a soil:solution of 1:5 after shaking for one hour, centrifuged at 5000 rpm for 5 min and then filtered through 0.2 mm cellulose membrane filter. Mehlich-3 extractant was used in this study because it has been recommended as a screening tool to estimate bioaccessible Pb (Minca et al., 2013). Three grams of dry soil was extracted with 25 ml of Mehlich-3 solution and filtered through 0.2 mm membrane filter to determine Mehlich-3 Pb. The Mehlich-3 solution was prepared in-house by mixing the following solutions; 0.2 N acetic acid, 0.25 N ammonium nitrate, 0.013 N nitric acid, 0.015 N ammonium fluoride and 0.001 M EDTA. All chemical analyses were performed following the QA/QC guidelines of NELAC-certified Laboratory at University of Florida using certified reference materials, spikes, duplicates, blanks and instrument calibration with standards.
Table 1 Selected soil characteristics of shooting range soils. Properties
SR 1
SR 2
SR 3
Total Pb (mg kg1) Soil pH CEC (Cmolc/Kg) Ox-Fe (mg kg1) Ox-Al (mg kg1) OM (%) Total Ca (mg kg1) % sand % silt % clay
12,689 ± 347 6.11 ± 0.15 24.8 ± 0.23 959 ± 92 278 ± 21 1.01 ± 0.05 1829 ± 45 86.6 9.46 3.93
70,350 ± 241 6.72 ± 0.15 11.1 ± 0.65 838 ± 26 162 ± 15 0.21 ± 0.02 900 ± 34 89.4 7.90 2.67
10,068 ± 234 6.68 ± 0.25 8.34 ± 0.48 379 ± 34 219 ± 23 0.67 ± 0.03 152 ± 13 88.0 7.07 4.96
CEC-cation exchange capacity; Ox-oxalate; OM-organic matter; SR-shooting range. Values are means ± standard error, n ¼ 4, .Error includes instrumental error, instrumental drift error, analytical error.
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2.3. Statistical analysis The experiment is a 3 2 2 factorial experiment. There are 3 different SR soils, two soil types (sieved and unsieved) and two plant cover (unvegetated and vegetated) with four replications arranged in a randomized complete block design. Treatment effects were determined by analysis of variance (ANOVA) followed by mean separation using the SAS software (SAS Institute, 2003). Linear correlation coefficients were also computed for various parameters using the SAS software. 3. Results and discussion 3.1. Soil characteristics Selected soil properties of the three SR are shown in Table 1. Total Pb concentrations of the sites ranged from 1% to 7% and followed the trend SR2 > SR1 > SR3. The three SR soils are sandy soils from Florida with low organic matter content. SR1 has the highest organic matter content, highest oxalate Fe/Al and CEC, SR2 has the highest soil pH and SR3 has the lowest CEC and oxalate Fe. SR1 had bullet mass of 106e114 g kg1; SR2 had bullet mass of 171e174 g kg1, SR3 had bullet mass of 113e152 g kg1 Chen and Daroub (2002) reported lead bullets weighing 180 g kg1 soil in the mid-berm of a 14 year old SR. Astrup et al. (1999) reported a bullet mass of 400 g kg1 soil in a 30 year old SR. In this study, SR2 had the highest bullet mass which corresponds to its extremely high total soil Pb concentration. 3.2. Effect of bullet removal on bioavailability of Pb in shooting range soils Bioavailability is a better estimate of environmental risk and metal toxicity than total concentrations (Hettiarachchi and Pierzynski, 2004). In this study, the effect of bullet removal on both the total and bioavailable Pb of contaminated shooting range soils was evaluated. Total soil Pb (Table 2) of sieved soils was significantly lower than unsieved soils except in the unvegetated SR2 soils. This is contrary to previous studies in shooting range soils. Liu et al. (2013) and Yin et al. (2010) reported that mechanical removal of bullets in the field increased total Pb content of the soil by converting metallic Pb from the bullet to the soil fraction. However, sieving removes the source of contamination, which may reduce contamination after a long period of time. The differences in results may be partly due to the presence of plants in this study. Additionally, in this study, sieving was done by hand while theirs was mechanical sieving. Bioavailability was measured with Mehlich-3 extraction and
plant Pb uptake in this study. Both Mehlich-3 Pb and plant uptake had the same trend; SR2 > SR1 > SR3. The aspect of plant uptake will be discussed in details later in the paper. Mehlich-3 Pb (Table 2) had the same trend as the total Pb in the soil and consistently extracted 25.3%e28.1% of the total soil Pb concentration in SR1; 25.1%e28.8% Pb in SR2 and 26.3e31.3% Pb in SR3. Mehlich-3 extractable Pb also had a positive correlation with both total plant Pb uptake (p < 0.05, r ¼ 0.47, n ¼ 24) and DOC (p < 0.001, r ¼ 0.46, n ¼ 48). In un-vegetated (control) soils, bullet removal increased the bioavailability of Pb with sieved soils having higher Mehlich-3 Pb than unsieved soils with bullets. The removal of bullets may have reduced toxicity of Pb to soil microbes which could lead to higher microbial activity and higher Pb bioavailability (Mehlich-3Pb). Liao et al. (2005) showed that microbial community structure and functional diversity were negatively affected by elevated metal levels. Mühlbachov a et al. (2005) reported a significant relationship between available metal concentrations and microbial activity. Microbial reduction of metals to a lower redox state may also result in reduced mobility and toxicity (Violante et al., 2010). In vegetated soils, sieving had no significant effect on Mehlich-3 Pb of SR1; increased Mehlich-3 Pb in SR2 soils while it reduced Mehlich-3 Pb in SR3 soils. This result may be due to differences in plant-soil interactions in the three different shooting range soils, since they are all vegetated soils. 3.3. Effect of bullet removal and vegetation on leachability of Pb in shooting range soils Total Pb leached from the three SR soils was in the order; SR3 > SR1 > SR2. The very low leaching of Pb in SR2 suggests a high buffering capacity of the soils. The high leaching of Pb in SR3 soils may be due to the very low CEC and oxalate extractable Fe in the soil. It has been reported that soils with high CEC and Fe have higher sorption affinities for Pb (Strawn and Sparks, 1999; Okkenhaug et al., 2016). Bullet removal increased total leachate Pb (Table 3) in SR1 and SR3 while it reduced total leachate Pb in SR2. The increased DOC production after bullet removal in all soils may be responsible for complexation and solubilization of Pb which increased leaching in sieved soils. This is consistent with previous studies that suggested that mobilization of Pb in SR soils was through enhanced solubilization of organic Pb complexes (Cao et al., 2003b). Since, a very high proportion (70%e88%) of total DOC was leached in the first two weeks of planting, with a general decline in DOC after two weeks; the decrease in Pb leached in SR1 and SR3 soils after 2 or 4 weeks after planting (WAP) may be due to the decline in DOC concentrations. On the contrary, the increased leaching of Pb in SR2 after 2 WAP
Table 2 Effect of sieving and vegetation on soil characteristics. Range
SR 1 Grass
Total soil Pb (mg/kg) Unsieved 20,759 ± 8328a Sieved 18,938 ± 5748b Soil pH Unsieved 5.74 ± 0.03a Sieved 5.92 ± 0.05b Mehlich-3 Pb (mg/kg) Unsieved 3570 ± 154a Sieved 3502 ± 155a
SR 2
SR 3
Control
Grass
Control
Grass
Control
15,344 ± 1218a 10,067 ± 1611b
60,339 ± 3630a 50,902 ± 1409b
56,657 ± 5811a 73,917 ± 7675b
9804 ± 1053a 8455 ± 1549a
13,202 ± 2974a 9289 ± 369b
6.11 ± 0.03a 6.05 ± 0.08a
5.92 ± 0.05a 5.64 ± 0.06b
5.50 ± 0.06a 4.78 ± 0.21b
5.30 ± 0.04a 4.84 ± 0.09b
5.50 ± 0.06a 5.59 ± 0.04b
3215 ± 117a 3490 ± 37b
17,677 ± 1156a 19,142 ± 492b
19,062 ± 704a 20,235 ± 618b
3135 ± 40a 2699 ± 94b
2986 ± 76b 3164 ± 41a
Values are means ± standard error, n ¼ 4, .Error includes instrumental error, instrumental drift error, analytical error. Treatments with different letters are significantly different at a ¼ 0.05; SR e Shooting range, control e un-vegetated soils.
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Table 3 Effect of sieving and vegetation on leachate characteristics. Range
SR 1 Grass
Total leachate Pb (mg/L) Unsieved 11.4 ± 1.89a Sieved 17.5 ± 3.17b Total DOC (mg/L) Unsieved 590 ± 4.44a Sieved 777 ± 8.53b Leachate pH Unsieved 6.75 ± 0.54a Sieved 7.32 ± 0.11b
SR 2
SR 3
Control
Grass
Control
Grass
Control
13.9 ± 3.00a 19.9 ± 1.94b
1.86 ± 0.45a 1.30 ± 0.12b
1.42 ± 0.04a 1.10 ± 0.10b
40.0 ± 13.6a 61.0 ± 17.0b
129 ± 32.0a 163 ± 26.0b
634 ± 50.4a 818 ± 19.6b
700 ± 7.14a 777 ± 36.8b
989 ± 73.5a 1032 ± 136a
481 ± 15.2a 526 ± 35.8b
583 ± 16.2a 777 ± 26.1b
6.24 ± 0.14a 6.15 ± 0.28a
7.58 ± 0.10a 7.68 ± 0.25a
7.56 ± 0.23a 7.61 ± 0.13a
6.96 ± 0.22a 6.12 ± 0.34b
5.51 ± 0.44a 5.70 ± 0.43a
Values are means ± standard error, n ¼ 4, Error includes instrumental error, instrumental drift error, analytical error. Treatments with different letters are significantly different at a ¼ 0.05; SR e Shooting range, control e un-vegetated soils.
may also be due to the decline in DOC produced in the soil. Though correlation analysis showed no significant relationship between leachate Pb and DOC, they were positive values for SR1 and SR3 while it was negative for SR2 soils. These results suggest that complexation and solubilization of Pb is probably occurring in SR1 and SR3 soils while adsorption may be the dominant mechanism in SR2 soil. Previous studies have reported that the following reactions control metal availability in the soil; adsorption, desorption, complexation and redox reactions (Violante et al., 2010; Hernandez-Soriano and Jimenez-Lopez, 2012). However, vegetated soils had lower Pb leached than unvegetated SR1 and SR3 soils. Table 3 shows that higher amounts of Pb were leached in these two soils from both vegetated and unvegetated soils than SR 2 soils. The reduced leaching of Pb in vegetated SR1 and SR3 soils may be partly due to plant uptake. Approximately 0.57e0.60 g Pb/plant was removed in SR1 while 0.47e0.55 g Pb/plant was removed in SR3 soils. 3.4. Effect of bullet removal and vegetation on water soluble Pb The effect of bullet removal on water-soluble Pb (bulk soil) was different in each shooting range soil. In vegetated soils, sieving significantly decreased water-soluble Pb in SR3 soil; increased water-soluble Pb in SR1 and had no significant effect on watersoluble Pb in SR2 (Fig. 1). In un-vegetated soils, sieving significantly decreased water-soluble Pb in SR2 soil while it increased water-soluble Pb in SR1 and SR3. Vegetation increased the water soluble Pb of sieved SR1 and SR2 and un-sieved SR2 and SR3. Howard et al. (2013) explained that the origin and mobilization of water-soluble Pb is complex and probably includes solubilized
Fig. 1. Water soluble Pb of the rhizosphere and bulk soil of shooting range soils with grasses. R-rhizosphere soil, B-bulk soil, SR-shooting range. Bars are standard error of means of 4 replicates. Error includes instrumental error, instrumental drift error, and analytical error. Treatments with different letters are significantly different at P 0.05.
colloidal organo-metallic complexes. However, there was no significant relationship between DOC and water-soluble Pb for all three soils suggesting that the origin of water-soluble Pb was probably not from DOC in this study. The total DOC leached in 8 weeks from un-vegetated soils was significantly (p < 0.05) higher than in vegetated soils suggesting that presence of plants was not majorly responsible for DOC production. The leachate pH (Table 3) of un-vegetated soils was also lower than vegetated soils probably due to higher production of organic acids in DOC. This is consistent with previous reports that plant roots contribute little to DOC production in the soil while microbial activity may contribute more to DOC production (Hagedorn et al., 2004; Malik and Gleixner, 2013). 3.5. Phytoavailability of Pb in rhizosphere and bulk soils Since, the rhizosphere has been defined as an important small biosphere with different physicochemical properties caused by exudation of low molecular weight organic acids by plant roots (Wang et al., 2002); it is expected that the rhizosphere soil will be acidic. However, rhizosphere soil of sieved SR2 and 3 had higher soil pH than the bulk soil (data not shown). Similarly, the rhizosphere soil of un-sieved SR1 and SR3 soil had higher soil pH than the bulk soil. Root exudation in the rhizosphere can lead to a higher soil pH resulting in increased weathering of Pb. The organic acids exuded in the rhizosphere can exacerbate the weathering of Pb in SR soils. Ma et al. (2007) reported that the weathering of Pb in SR soils leads to an increase in soil pH. This may explain why the presence of bullets increased soil pH of the rhizosphere soils of SR1 and SR3 and the bulk soil of SR2 and SR3. The water-soluble Pb in the rhizosphere of SR2 was six to eight times more than the water-soluble Pb of the bulk soil. SR2 had the highest plant Pb uptake (Table 4) in both sieved and un-sieved soils despite its very low water-soluble Pb in the bulk soil because the plant was able to mobilize Pb in its rhizosphere. This also explains why vegetation did not reduce leaching of Pb in SR2 soils. The grasses in SR2 were probably not able to take up all the Pb mobilized in the rhizosphere and bulk soils. The water soluble Pb of the rhizosphere soils had a positive correlation (p < 0.01, r ¼ 0.58, n ¼ 24) with plant Pb uptake while water-soluble Pb of the bulk soil had no relationship with plant uptake indicating that the plant Pb uptake was from the rhizosphere Pb pool. The rhizosphere watersoluble Pb of SR3 was close to that of the bulk soil in sieved soils suggesting some amount of root exudation. 3.6. Plant Pb uptake and plant biomass of St. Augustine grass Another way to measure bioavailability is through plant uptake
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Table 4 Effect of bullet removal on plant Pb uptake and biomass of St. Augustine grass. SR 1 Shoot
SR 2
SR 3
Root
Shoot
Root
Shoot
Root
1988 ± 364a 2050 ± 292a
580 ± 190a 880 ± 108b
2065 ± 399a 5021 ± 1174b
268 ± 20.5a 252 ± 55a
2068 ± 96.5a 1893 ± 99.5b
174 ± 9.5a 162 ± 7.50a
40 ± 2.46a 59.3 ± 16.7b
194 ± 20.3a 156 ± 14.8b
58.4 ± 3.21a 56.9 ± 4.14a
179 ± 10.6a 159 ± 11.6b
1
Plant Pb uptake (mg kg ) Unsieved 396 ± 71a Sieved 367 ± 109a Plant biomass (g) Unsieved 74.7 ± 6a Sieved 72 ± 5a
Values are means ± standard error, n ¼ 4, .Error includes instrumental error, instrumental drift error, analytical error. SR-shooting range, WAP-weeks after planting, Shoot-aboveground biomass. Treatments followed by same letters are not significantly different at a ¼ 0.05.
since bioavailability has been defined as the proportion of total metals that are available for incorporation into biota which includes plants (John and Leventhal, 1995). The soil pH of vegetated soils was lower than un-vegetated soils in SR1 and SR3 while it was higher in SR2 soils suggesting that the grasses had an acidifying effect in SR1 and SR3. The presence of grasses can increase bioavailability by increasing acidity via processes like root exudation, acidifying effects of CO2 produced in root respiration and Hþ released due to cationic nutrient intake (Levonmaki et al., 2006). Even though plants have mechanisms for increasing metal bioavailability, the high plant Pb uptake recorded in this study showed high bioavailability of Pb in shooting range soils. The plant Pb uptake (Table 4) of St. Augustine grass was comparable and even higher than what is found in the literature. Total plant Pb in grasses ranged from 2145 mg kg1 to 5901 mg kg1 Pb with grasses in SR2 having the highest Pb uptake both in the aboveground (shoots) and belowground (roots) biomass. Pb concentrations in the aboveground biomass ranged from 252 mg kg1 to 880 mg kg1 Pb while root Pb concentrations ranged from 1893 mg kg1 to 5021 mg kg1 Pb. Root Pb concentration of St. Augustine grass was significantly higher than the Pb concentrations in aboveground biomass with about 74e93% of total plant Pb in the roots. Plant roots have the effect of stabilizing Pb in the surrounding soil and Pb retention in the roots is believed to be based on the binding of Pb to ion exchangeable sites on the cell wall and extracellular precipitation (Sharma and Dubey, 2005). Previous studies have reported lower plant Pb concentrations for St. Augustine grass. Cao et al. (2002) reported root concentrations between 110 mg kg1 and 981 mg kg1 and aboveground concentrations between 20 mg kg1 and 77 mg kg1 for St. Augustine grass growing in a battery recycling and salvage yard. Xia (2004) reported even lower concentrations that ranged from 0.44 to 0.66 mg kg1 in roots and 0.41e0.51 mg kg1 for aboveground concentrations of St. Augustine grass growing in a waste dump. St. Augustine grass growing in a metal contaminated site in Florida had 30.8 mg kg1 Pb in the roots and 14 mg kg1 Pb in the above ground biomass (Yoon et al., 2006). Cao et al. (2003b) reported that Pb concentrations in the aboveground biomass was 805 mg kg1 and 1342 mg kg1 in roots of Bermuda grass growing in a shooting range facility. Plant Pb uptake of 1000e1700 mg kg1 was reported by Freitas et al. (2013) in a study where citric acid was used to assist the phytoextraction of Pb by maize and vetiver. St. Augustine took up more Pb without assistance by an acid. The effect of bullet removal on plant uptake had the same trend with that of Mehlich-3 Pb. Sieving had no significant effect in SR1; increased Pb uptake in root and shoot of grasses in SR2; and reduced root Pb uptake of grasses in SR3. The amount of DOC produced may be responsible since bullet removal increased DOC
production. The trend in DOC concentration and plant Pb uptake are the same; SR2 > SR1 > SR3. Plant biomass data (Table 4) showed that St. Augustine grass had higher root biomass in unsieved soils than sieved soils showing a high tolerance to the presence of bullets in the unsieved soil. The grass shows potential to be used in phytostabilization of Pb in contaminated soils. The vegetation of shooting ranges will lead to uptake and immobilization of Pb by plant roots which may help limit contaminant migration, provide ground cover from runoff and help beautify the environment at shooting ranges. 4. Conclusion Bullet removal reduced total soil Pb except in unvegetated SR2; increased bioavailability of Pb in un-vegetated soils; and increased DOC concentration in the leachates. Vegetation reduced leaching of Pb in SR1 and SR3 though a combination of bullet removal and vegetation significantly reduced leaching of Pb in SR2. Vegetation increased water soluble Pb thereby increasing Pb mobility in the soil. The addition of a chemical stabilizer to immobilize Pb may be the solution since vegetation is needed as ground cover. St Augustine grass accumulated high concentrations of Pb by increasing Pb availability in the rhizosphere. A very high proportion of the Pb in the grass was sequestered in the root showing great potentials to be used in phytostabilization of Pb. St Augustine grass had higher plant biomass in unsieved soils with bullets suggesting tolerance to Pb. Further studies may study anti-oxidative responses of St. Augustine grass to Pb toxicity in Pb contaminated soils. Acknowledgement The authors are grateful for the funding assistance from the Florida Department of Environment Protection. References Astrup, T., Boddum, J.K., Christensen, T.H., 1999. Lead distribution and mobility in a soil embankment used as a bullet stop at a shooting range. J. Soil Contam. 8, 653465. Beak, D.G., Basta, N.T., Scheckel, K.G., Traina, S.J., 2006. Bioaccessibility of Pb sequestered to corundum and ferrihydrite in a simulated gastrointestinal system. J. Environ. Qual. 35, 2075e2083. Butler, A., Martin, A., Larson, S., Fabian, G., Nestler, C., 2010. Treatment of metal contaminated soil by the application of lime and grasses. GeoFlorida 2010, 2801e2810. http://dx.doi.org/10.1061/41095(365)285. Cao, X., Ma, L.Q., Chen, M., Satya, P.S., Harris, W.G., 2002. Impacts of phosphate amendments on lead biogeochemistry at a contaminated site. USA. Environ. Sci. Technol. 36 (24), 5296e5304. Cao, R.X., Ma, L.Q., Singh, S.P., Chen, M., Harris, W., 2003a. Phosphate-induced metal immobilization in a contaminated site. Environ. Pollut. 122, 19e28. Cao, X., Ma, L.Q., Chen, M., Hardison, D.W., Harris, W.G., 2003b. Weathering of lead bullets and their environmental effects at outdoor shooting ranges. J. Environ. Qual. 307, 526e534. Chen, M., Daroub, S.H., 2002. Characterization of lead in soils of a rifle/pistol shooting range in central Florida. Soil Sediment Contam. 11 (1), 1e17.
A.O. Fayiga, U. Saha / Chemosphere 160 (2016) 252e257 Dermatas, D., Menounou, N., Dadachov, M., Dutko, P., Shen, G., Xu, X., Tsaneva, V., 2006. Lead leachability in firing range soils. Environ. Eng. Sci. 23 (1), 88e101. Fayiga, A.O., Saha, U., 2016. Soil pollution in outdoor shooting ranges: health effects, bioavailability and best management practices. Environ. Pollut. 216, 135e145. Fayiga, A.O., Saha, U., Cao, X., Ma, L.Q., 2011. Chemical and physical characterization of lead in three shooting range soils in Florida. Chem. Speciat. Bioavailab. 23 (3), 148e154. Freitas, E.V., Nascimento, C.W., Souza, A., Silva, F.B., 2013. Citric acid-assisted phytoextraction of lead: a field experiment. Chemosphere. http://dx.doi.org/10. 1016/j.chemosphere.2013.01.103. Hagedorn, F., Saurer, M., Blaser, P., 2004. A 13C tracer study to identify the origin of dissolved organic carbon in forested mineral soils. Eur. J. Soil Sci. 55 (1), 91e100. Hardison, D.W., Ma, L.Q., Luongo, T., Harris, W.G., 2004. Lead contamination in shooting range soils from abrasion of lead bullets and subsequent weathering. Sci. Total Environ. 328, 175e183. Hernandez-Soriano, M., Jimenez-Lopez, J., 2012. Effects of soil water content and organic matter addition on the speciation and bioavailability of heavy metals. Sci. Total Environ. 423, 55e61. Hettiarachchi, G.M., Pierzynski, G.M., 2004. Soil Pb bioavailability and in situ remediation of Pb contaminated soils: a review. Environ. Prog. 23 (1), 78e93. Houben, D., Pircar, J., Sonnet, P., 2012. Heavy metal immobilization by cost-effective amendments in a contaminated soil: effects on metal leaching and phytoavailability. J. Geochem. Explor. 123, 87e94. Howard, J.L., Dubay, B.R., Daniels, W.L., 2013. Artifacts weathering, anthropogenic microparticles and lead contamination in urban soils at former demolition sites, Detroit, Michigan. Environ. Pollut. 179, 1e12. John, D.A., Leventhal, J.S., 1995. Bioavailability of Metal. pubs.usgs.gov/of/1995/ofr95e0831/CHAP2.pdf. Levei, E., Miclean, M., Senila, M., Cadar, O., Roman, C., Micle, V., 2010. Assessment of Pb, Cu, and Zn availability for plants in Baia Mare mining region. J. Plant Dev. 17, 139e144. Levonmaki, M., Hartikainen, H., Kairesalo, T., 2006. Effect of organic amendment and plant roots on the solubility and mobilization of lead in soils at a shooting range. J. Environ. Qual. 35, 1026e1031. Liao, M., Chen, C.L., Huang, C.Y., 2005. Effect of heavy metals on soil microbial activity and diversity in a reclaimed mining wasteland of red soil area. J. Environ. Sci. 17 (5), 832e837. Liu, R., Gress, J., Gao, J., Ma, L.Q., 2013. Impacts of two best management practices on Pb weathering and leachability in shooting range soils. Environ. Monit. Assess. 12, 3039e3045. Ma, L.Q., Hardison, D.W., Harris, W.G., Cao, X., Qixing, Z., 2007. Effects of soil property and soil amendments on weathering of abraded metallic Pb in shooting ranges. Water Air Soil Pollut. 178, 297e307. Malik, A., Gleixner, G., 2013. Importance of microbial soil organic matter processing in dissolved organic carbon production. Fed. Eur. Microbiol. Soc. 86 (1), 139e148. McKeague, J.A., Day, J.H., 1966. Dithionite and oxalate extractable Fe and Al as aids in differentiating various classes of soils. Can. J. Soil Sci. 46, 1e22. McLaughlin, M.J., 2001. Ageing of Metals in Soil Changes Bioavailability. A
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Publication of the International Council on Metals and the Environment. Meers, E., Dulaing, G., Unamando, V.G., Lesage, E., Tack, F.M., Verloo, M.G., 2006. Water extractability of trace metals from soils. Some pitfalls. Water, Air, Soil Pollut. 176, 21e35. Minca, K.K., Basta, N.T., Scheckel, K.G., 2013. Using the Mehlich-3 soil test as an inexpensive screening tool to estimate total and bioaccessible lead in urban soils. J. Environ. Qual. 42 (5), 1518e1526. , G., Simon, , M., 2005. The availability of Cd, Pb and Zn and Mühlbachova T., Pechova their relationships with soil pH and microbial biomass in soils amended by natural clinoptilolite. Plant Soil Environ. 51 (1), 26e33. Okkenhaug, G., Gebhardt, K., Amstaetter, K., Bue, H., Herzel, H., Mariussen, E., Almås, A., Cornelissen, G., Breedveld, G., Rasmussen, G., Mulder, J., 2016. Antimony (Sb) and lead (Pb) in contaminated shooting range soils: Sb and Pb mobility and immobilization by iron based sorbents, a field study. J. Haz. Mat. 307, 336e343. O’Connor, G., Martin, W.A., Larson, S.L., Weiss, C., Malone, P., 2009. Distribution of tungsten on soil particles following firing of tungsten ammunition into various soil types. Land Contam. Reclam. 17, 67e73. Sanderson, P., Naidu, R., Bolan, N., 2014. Ecotoxicity of chemically stabilised metalloids in shooting range soils. Ecotoxicol. Environ. Saf. 100, 201e208. http://dx. doi.org/10.1016/j.ecoenv.2013.11.003. SAS, 2003. Statistical Analysis Institute, Inc.. Cary, NC, 27513. Sharma, P., Dubey, R.S., 2005. Lead toxicity in plants. Braz. J. Plant Physiology 17 (1), 35e52. Shu, W.R., Ye, Z.H., Lan, C.Y., Zhang, Z.Q., Wong, M.H., 2002. Lead, zinc, and copper accumulation and tolerance in populations of Paspalum distichum and Cynodon dactylon. Environ. Pollut. 120, 445e453. Siebielec, G., Chaney, R.L., 2012. Testing amendments for remediation of military range contaminated soil. J. Environ. Manag. 108, 8e13. Strawn, D., Sparks, D., 1999. The use of XAFS to distinguish between inner- and outer-sphere lead adsorption complexes on montmorillonite. J. Colloid Interface Sci. 216, 257e269. USEPA, 2005. Best Management Practices for Pb at Outdoor Shooting Ranges. EPA902-B-01e001. Revised June 2005. Region 2. Violante, A., Cozzolino, V., Perelomov, L., Caporale, A.G., Pigna, M., 2010. Mobility and bioavailability of heavy metals and metalloids in soil environments. J. Soil Sci. Plant Nutr. 10 (3), 268e292. Wang, Z., Xiao-Quan, S., Zhang, S., 2002. Comparison between fractionation and bioavailability of trace elements in rhizosphere and bulk soils. Chemosphere 46, 1163e1171. Xia, H.P., 2004. Ecological rehabilitation and phytoremediation with four grasses in oil shale mined land. Chemosphere 54, 345e353. Yin, X., Saha, U.K., Ma, L.Q., 2010. Effectiveness of best management practices in reducing Pb-bullet weathering in a shooting range in Florida. J. Haz. Mat. 179, 895e900. Yoon, J., Cao, X., Zhou, Q., Ma, L.Q., 2006. Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci. Total Environ. 368, 456e464.
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The effect of bullet removal and vegetation on mobility of Pb in shooting range soils Abioye O. Fayiga a, *, Uttam Saha a, b a b
Soil and Water Science Department, University of Florida, Gainesville, FL 32611-0290, USA University of Georgia Cooperative Extension, 2300 College Station Road, Athens, GA 30602, USA
h i g h l i g h t s
g r a p h i c a l a b s t r a c t
Two best management practices for shooting ranges, bullet removal and vegetation, were evaluated in a green house study. Bullet removal reduced total soil Pb and increased DOC in leachates. Bullet removal increased bioavailable Pb in un-vegetated soils. Vegetation reduced leaching of Pb in two shooting range soils. St. Augustine grass accumulated up to 5021 mg Pb/kg in roots.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 March 2016 Received in revised form 19 June 2016 Accepted 26 June 2016 Available online 6 July 2016
Lead (Pb) contamination at shooting ranges is a public health concern because Pb is a toxic metal. An experiment was conducted to determine the effect of two best management practices; bullet removal and vegetation, on bioavailability and leachability of Pb in three shooting range (SR) soils. St. Augustine grass was grown in sieved (2 mm) and un-sieved SR soils for 8 weeks after which leachates, soil and plant samples were analyzed. Bullet removal reduced total soil Pb, increased Mehlich-3 Pb in unvegetated soils and increased dissolved organic carbon (DOC) in all soils. Bullet removal increased leaching in two SR soils while grasses reduced leaching but increased water soluble Pb in two SR soils. The roots of the grasses were able to accumulate more Pb in the root (1893e5021 mg kg1) than the aboveground biomass (252e880 mg kg1) due to mobilization of Pb in the rhizosphere. Grasses had a higher plant biomass in unsieved soils suggesting tolerance to the presence of bullets in the unsieved soils. Results suggest that bullet removal probably increased microbial activity and Pb bioavailability in the soil. The leaching and bioavailability of Pb in shooting range soils depends on biological activities and chemical processes in the soil. © 2016 Elsevier Ltd. All rights reserved.
Handling Editor: Martine Leermakers Keywords: Shooting ranges Pb St. Augustine grass Dissolved organic carbon Rhizosphere Mehlich-3 Pb
1. Introduction Soil contamination with lead (Pb) has been reported in shooting ranges (SR) worldwide (Dermatas et al., 2006; Siebielec and
* Corresponding author. E-mail address: [email protected] (A.O. Fayiga). http://dx.doi.org/10.1016/j.chemosphere.2016.06.098 0045-6535/© 2016 Elsevier Ltd. All rights reserved.
Chaney, 2012; Sanderson et al., 2014). Approximately 80,000 tons/year of Pb was used in the production of bullets and shot in the United States in the late 1990s (USEPA, 2005; Hardison et al., 2004). Bullets are fragmented and pulverized upon impact with ground, backstop, berms or bullet trap at SR (O’Connor et al., 2009). It has been reported that soil and Pb metallic fragment particle sizes play a dominant role in the rate and amount of Pb release in SR soils
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(Dermatas et al., 2006). Weathering of fragmented Pb bullets eventually results in elevated total Pb concentrations in SR soils especially those that have been in operation for a long period of time. Some of the best management practices (BMP) used to mitigate Pb contamination in SR includes sieving to remove the bullet fragments and vegetation to provide a cover for the soil (USEPA, 2005). Removal of used bullets from contaminated SR soils is expected to reduce Pb contamination at these sites. However, previous studies have reported that the abrasive action of mechanical sieving transferred metallic Pb to the soil fraction (<2 mm) and increased total Pb in the soil (Yin et al., 2010; Liu et al., 2013). It is imperative to evaluate the effect of bullet removal on Pb bioavailability since total concentrations do not provide adequate information on toxicity of heavy metals to the users and biota at these sites. The total amount of metals in the soil is not available because they are adsorbed or bound by organic and inorganic solid phases in the soil such as organic matter, Fe and Al oxides and clay minerals (Fayiga and Saha, 2016). Since bioavailability is the portion that is available or can be absorbed by living organisms, it is a better estimate of environmental risk and toxicity (McLaughlin, 2001; Hettiarachchi and Pierzynski, 2004). The speciation of Pb is also important because it’s the key to understanding the fate and bioavailability of Pb in the environment (Beak et al., 2006). Water-soluble concentration has also been said to be the most eco-toxicologically relevant fraction in the environment due to its high contamination potential of the surface and ground water through leaching and runoff (Meers et al., 2006; Levei et al., 2010). It may also control plant uptake in vegetated soils. The presence of vegetation in SR is significant because some plants are tolerant to metals and can immobilize contaminants in the root zone (Cao et al., 2003a). The metal tolerant plants can be used for revegetation of contaminated sites (Shu et al., 2002). Butler et al. (2010) reported that vegetation alone reduced metal concentrations in run-off water by about nine times compared to the control. The combination of vegetation (Houben et al., 2012) and bullet removal in SR may be a cost efficient and sustainable method of remediation for contaminated SR soils. Therefore, the objectives of this study were to determine the effect of bullet removal and vegetation on Pb leachability and bioavailability in SR soils. 2. Materials and method 2.1. Experimental set up The soils used in this experiment were collected from the berms of three rifle shooting ranges (SR1, SR2 and SR3) in Florida. SR1 has been in operation for 6 years whereas the SR2 and SR3 have been in operation for 15 and 30 years respectively. We took random samples from top, bottom and middle of the berms and mixed them up to make a representative 100 kg composite sample. The soils were hand mixed and air-dried for a week, with 50 kg passed through a 2-mm sieve (no bullets), while the other 50 kg was not sieved (with bullets). Shooting range soil weighing 1.6 kg was thoroughly hand mixed with 2 g of slow release fertilizer (18-9-18, N-P2O5-K2O) and placed in a plastic pot with a diameter of 0.14 m and height 0.16 m (2.5 L). One plug of St. Augustine grass (Stenotaphrum secundatum) was planted in pots containing sieved or un-sieved soil, with soil alone as controls with four replications. The plants were grown in the University of Florida greenhouse where the average temperature ranged from 14 (night) to 30 C (day), with an average photosynthetic photon flux density of 825 mmol m2 s1. The plants were watered with deionized water and a petri dish was placed under
253
each pot to collect potential leachates during the experiment. Leachate was collected every two weeks and analyzed for pH, DOC and Pb content. The grasses were harvested after 8 weeks and separated into aboveground and belowground biomass (roots). Fresh plant samples were rinsed with deionized water, dried in the oven for 3 days at 65 C and then ground in a mill. The weights of fresh and dry biomass of grass in each pot were determined. Soil samples were collected after harvesting and analyzed for pH, water-soluble Pb, Mehlich-3-Pb and total Pb. Rhizosphere soil collected from the roots was separated from the bulk soil and analyzed for water-soluble Pb and soil pH. Unsieved soils were sieved after harvest and bullet mass determined.
2.2. Chemical analysis Characterization of sieved soils were done before the experiment by routinely analyzing for CEC, organic matter, particle size distribution, soil pH and water soluble Pb. Detailed methods of analysis can be found in a previous publication (Fayiga et al., 2011). Non-crystalline aluminum and iron in the soils were extracted by shaking 2 g soil in 10 ml acid ammonium oxalate for 4 h in the dark (McKeague and Day, 1966). Fe and Al in the extract were measured by using a flame atomic absorption spectrophotometer (FAAS, Varian 220 FS with SIPS, Walnut Creek, CA). Results are presented in Table 1. Soil and plant samples from experiment were digested with nitric acid and hydrogen peroxide using the Hot Block Digestion System (Environmental Express, Mt. Pleasant, SC; EPA Method 3050a). Total Pb contents of soil/plant digest; filtrate/extracts and leachates were analyzed on FAAS. Dissolved organic carbon in leachates from soils was analyzed using a total organic carbon analyzer (TOC-5050 A, Shimadzu Corporation, Japan) which was calibrated with standards. Watersoluble Pb was determined in a soil:solution of 1:5 after shaking for one hour, centrifuged at 5000 rpm for 5 min and then filtered through 0.2 mm cellulose membrane filter. Mehlich-3 extractant was used in this study because it has been recommended as a screening tool to estimate bioaccessible Pb (Minca et al., 2013). Three grams of dry soil was extracted with 25 ml of Mehlich-3 solution and filtered through 0.2 mm membrane filter to determine Mehlich-3 Pb. The Mehlich-3 solution was prepared in-house by mixing the following solutions; 0.2 N acetic acid, 0.25 N ammonium nitrate, 0.013 N nitric acid, 0.015 N ammonium fluoride and 0.001 M EDTA. All chemical analyses were performed following the QA/QC guidelines of NELAC-certified Laboratory at University of Florida using certified reference materials, spikes, duplicates, blanks and instrument calibration with standards.
Table 1 Selected soil characteristics of shooting range soils. Properties
SR 1
SR 2
SR 3
Total Pb (mg kg1) Soil pH CEC (Cmolc/Kg) Ox-Fe (mg kg1) Ox-Al (mg kg1) OM (%) Total Ca (mg kg1) % sand % silt % clay
12,689 ± 347 6.11 ± 0.15 24.8 ± 0.23 959 ± 92 278 ± 21 1.01 ± 0.05 1829 ± 45 86.6 9.46 3.93
70,350 ± 241 6.72 ± 0.15 11.1 ± 0.65 838 ± 26 162 ± 15 0.21 ± 0.02 900 ± 34 89.4 7.90 2.67
10,068 ± 234 6.68 ± 0.25 8.34 ± 0.48 379 ± 34 219 ± 23 0.67 ± 0.03 152 ± 13 88.0 7.07 4.96
CEC-cation exchange capacity; Ox-oxalate; OM-organic matter; SR-shooting range. Values are means ± standard error, n ¼ 4, .Error includes instrumental error, instrumental drift error, analytical error.
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2.3. Statistical analysis The experiment is a 3 2 2 factorial experiment. There are 3 different SR soils, two soil types (sieved and unsieved) and two plant cover (unvegetated and vegetated) with four replications arranged in a randomized complete block design. Treatment effects were determined by analysis of variance (ANOVA) followed by mean separation using the SAS software (SAS Institute, 2003). Linear correlation coefficients were also computed for various parameters using the SAS software. 3. Results and discussion 3.1. Soil characteristics Selected soil properties of the three SR are shown in Table 1. Total Pb concentrations of the sites ranged from 1% to 7% and followed the trend SR2 > SR1 > SR3. The three SR soils are sandy soils from Florida with low organic matter content. SR1 has the highest organic matter content, highest oxalate Fe/Al and CEC, SR2 has the highest soil pH and SR3 has the lowest CEC and oxalate Fe. SR1 had bullet mass of 106e114 g kg1; SR2 had bullet mass of 171e174 g kg1, SR3 had bullet mass of 113e152 g kg1 Chen and Daroub (2002) reported lead bullets weighing 180 g kg1 soil in the mid-berm of a 14 year old SR. Astrup et al. (1999) reported a bullet mass of 400 g kg1 soil in a 30 year old SR. In this study, SR2 had the highest bullet mass which corresponds to its extremely high total soil Pb concentration. 3.2. Effect of bullet removal on bioavailability of Pb in shooting range soils Bioavailability is a better estimate of environmental risk and metal toxicity than total concentrations (Hettiarachchi and Pierzynski, 2004). In this study, the effect of bullet removal on both the total and bioavailable Pb of contaminated shooting range soils was evaluated. Total soil Pb (Table 2) of sieved soils was significantly lower than unsieved soils except in the unvegetated SR2 soils. This is contrary to previous studies in shooting range soils. Liu et al. (2013) and Yin et al. (2010) reported that mechanical removal of bullets in the field increased total Pb content of the soil by converting metallic Pb from the bullet to the soil fraction. However, sieving removes the source of contamination, which may reduce contamination after a long period of time. The differences in results may be partly due to the presence of plants in this study. Additionally, in this study, sieving was done by hand while theirs was mechanical sieving. Bioavailability was measured with Mehlich-3 extraction and
plant Pb uptake in this study. Both Mehlich-3 Pb and plant uptake had the same trend; SR2 > SR1 > SR3. The aspect of plant uptake will be discussed in details later in the paper. Mehlich-3 Pb (Table 2) had the same trend as the total Pb in the soil and consistently extracted 25.3%e28.1% of the total soil Pb concentration in SR1; 25.1%e28.8% Pb in SR2 and 26.3e31.3% Pb in SR3. Mehlich-3 extractable Pb also had a positive correlation with both total plant Pb uptake (p < 0.05, r ¼ 0.47, n ¼ 24) and DOC (p < 0.001, r ¼ 0.46, n ¼ 48). In un-vegetated (control) soils, bullet removal increased the bioavailability of Pb with sieved soils having higher Mehlich-3 Pb than unsieved soils with bullets. The removal of bullets may have reduced toxicity of Pb to soil microbes which could lead to higher microbial activity and higher Pb bioavailability (Mehlich-3Pb). Liao et al. (2005) showed that microbial community structure and functional diversity were negatively affected by elevated metal levels. Mühlbachov a et al. (2005) reported a significant relationship between available metal concentrations and microbial activity. Microbial reduction of metals to a lower redox state may also result in reduced mobility and toxicity (Violante et al., 2010). In vegetated soils, sieving had no significant effect on Mehlich-3 Pb of SR1; increased Mehlich-3 Pb in SR2 soils while it reduced Mehlich-3 Pb in SR3 soils. This result may be due to differences in plant-soil interactions in the three different shooting range soils, since they are all vegetated soils. 3.3. Effect of bullet removal and vegetation on leachability of Pb in shooting range soils Total Pb leached from the three SR soils was in the order; SR3 > SR1 > SR2. The very low leaching of Pb in SR2 suggests a high buffering capacity of the soils. The high leaching of Pb in SR3 soils may be due to the very low CEC and oxalate extractable Fe in the soil. It has been reported that soils with high CEC and Fe have higher sorption affinities for Pb (Strawn and Sparks, 1999; Okkenhaug et al., 2016). Bullet removal increased total leachate Pb (Table 3) in SR1 and SR3 while it reduced total leachate Pb in SR2. The increased DOC production after bullet removal in all soils may be responsible for complexation and solubilization of Pb which increased leaching in sieved soils. This is consistent with previous studies that suggested that mobilization of Pb in SR soils was through enhanced solubilization of organic Pb complexes (Cao et al., 2003b). Since, a very high proportion (70%e88%) of total DOC was leached in the first two weeks of planting, with a general decline in DOC after two weeks; the decrease in Pb leached in SR1 and SR3 soils after 2 or 4 weeks after planting (WAP) may be due to the decline in DOC concentrations. On the contrary, the increased leaching of Pb in SR2 after 2 WAP
Table 2 Effect of sieving and vegetation on soil characteristics. Range
SR 1 Grass
Total soil Pb (mg/kg) Unsieved 20,759 ± 8328a Sieved 18,938 ± 5748b Soil pH Unsieved 5.74 ± 0.03a Sieved 5.92 ± 0.05b Mehlich-3 Pb (mg/kg) Unsieved 3570 ± 154a Sieved 3502 ± 155a
SR 2
SR 3
Control
Grass
Control
Grass
Control
15,344 ± 1218a 10,067 ± 1611b
60,339 ± 3630a 50,902 ± 1409b
56,657 ± 5811a 73,917 ± 7675b
9804 ± 1053a 8455 ± 1549a
13,202 ± 2974a 9289 ± 369b
6.11 ± 0.03a 6.05 ± 0.08a
5.92 ± 0.05a 5.64 ± 0.06b
5.50 ± 0.06a 4.78 ± 0.21b
5.30 ± 0.04a 4.84 ± 0.09b
5.50 ± 0.06a 5.59 ± 0.04b
3215 ± 117a 3490 ± 37b
17,677 ± 1156a 19,142 ± 492b
19,062 ± 704a 20,235 ± 618b
3135 ± 40a 2699 ± 94b
2986 ± 76b 3164 ± 41a
Values are means ± standard error, n ¼ 4, .Error includes instrumental error, instrumental drift error, analytical error. Treatments with different letters are significantly different at a ¼ 0.05; SR e Shooting range, control e un-vegetated soils.
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Table 3 Effect of sieving and vegetation on leachate characteristics. Range
SR 1 Grass
Total leachate Pb (mg/L) Unsieved 11.4 ± 1.89a Sieved 17.5 ± 3.17b Total DOC (mg/L) Unsieved 590 ± 4.44a Sieved 777 ± 8.53b Leachate pH Unsieved 6.75 ± 0.54a Sieved 7.32 ± 0.11b
SR 2
SR 3
Control
Grass
Control
Grass
Control
13.9 ± 3.00a 19.9 ± 1.94b
1.86 ± 0.45a 1.30 ± 0.12b
1.42 ± 0.04a 1.10 ± 0.10b
40.0 ± 13.6a 61.0 ± 17.0b
129 ± 32.0a 163 ± 26.0b
634 ± 50.4a 818 ± 19.6b
700 ± 7.14a 777 ± 36.8b
989 ± 73.5a 1032 ± 136a
481 ± 15.2a 526 ± 35.8b
583 ± 16.2a 777 ± 26.1b
6.24 ± 0.14a 6.15 ± 0.28a
7.58 ± 0.10a 7.68 ± 0.25a
7.56 ± 0.23a 7.61 ± 0.13a
6.96 ± 0.22a 6.12 ± 0.34b
5.51 ± 0.44a 5.70 ± 0.43a
Values are means ± standard error, n ¼ 4, Error includes instrumental error, instrumental drift error, analytical error. Treatments with different letters are significantly different at a ¼ 0.05; SR e Shooting range, control e un-vegetated soils.
may also be due to the decline in DOC produced in the soil. Though correlation analysis showed no significant relationship between leachate Pb and DOC, they were positive values for SR1 and SR3 while it was negative for SR2 soils. These results suggest that complexation and solubilization of Pb is probably occurring in SR1 and SR3 soils while adsorption may be the dominant mechanism in SR2 soil. Previous studies have reported that the following reactions control metal availability in the soil; adsorption, desorption, complexation and redox reactions (Violante et al., 2010; Hernandez-Soriano and Jimenez-Lopez, 2012). However, vegetated soils had lower Pb leached than unvegetated SR1 and SR3 soils. Table 3 shows that higher amounts of Pb were leached in these two soils from both vegetated and unvegetated soils than SR 2 soils. The reduced leaching of Pb in vegetated SR1 and SR3 soils may be partly due to plant uptake. Approximately 0.57e0.60 g Pb/plant was removed in SR1 while 0.47e0.55 g Pb/plant was removed in SR3 soils. 3.4. Effect of bullet removal and vegetation on water soluble Pb The effect of bullet removal on water-soluble Pb (bulk soil) was different in each shooting range soil. In vegetated soils, sieving significantly decreased water-soluble Pb in SR3 soil; increased water-soluble Pb in SR1 and had no significant effect on watersoluble Pb in SR2 (Fig. 1). In un-vegetated soils, sieving significantly decreased water-soluble Pb in SR2 soil while it increased water-soluble Pb in SR1 and SR3. Vegetation increased the water soluble Pb of sieved SR1 and SR2 and un-sieved SR2 and SR3. Howard et al. (2013) explained that the origin and mobilization of water-soluble Pb is complex and probably includes solubilized
Fig. 1. Water soluble Pb of the rhizosphere and bulk soil of shooting range soils with grasses. R-rhizosphere soil, B-bulk soil, SR-shooting range. Bars are standard error of means of 4 replicates. Error includes instrumental error, instrumental drift error, and analytical error. Treatments with different letters are significantly different at P 0.05.
colloidal organo-metallic complexes. However, there was no significant relationship between DOC and water-soluble Pb for all three soils suggesting that the origin of water-soluble Pb was probably not from DOC in this study. The total DOC leached in 8 weeks from un-vegetated soils was significantly (p < 0.05) higher than in vegetated soils suggesting that presence of plants was not majorly responsible for DOC production. The leachate pH (Table 3) of un-vegetated soils was also lower than vegetated soils probably due to higher production of organic acids in DOC. This is consistent with previous reports that plant roots contribute little to DOC production in the soil while microbial activity may contribute more to DOC production (Hagedorn et al., 2004; Malik and Gleixner, 2013). 3.5. Phytoavailability of Pb in rhizosphere and bulk soils Since, the rhizosphere has been defined as an important small biosphere with different physicochemical properties caused by exudation of low molecular weight organic acids by plant roots (Wang et al., 2002); it is expected that the rhizosphere soil will be acidic. However, rhizosphere soil of sieved SR2 and 3 had higher soil pH than the bulk soil (data not shown). Similarly, the rhizosphere soil of un-sieved SR1 and SR3 soil had higher soil pH than the bulk soil. Root exudation in the rhizosphere can lead to a higher soil pH resulting in increased weathering of Pb. The organic acids exuded in the rhizosphere can exacerbate the weathering of Pb in SR soils. Ma et al. (2007) reported that the weathering of Pb in SR soils leads to an increase in soil pH. This may explain why the presence of bullets increased soil pH of the rhizosphere soils of SR1 and SR3 and the bulk soil of SR2 and SR3. The water-soluble Pb in the rhizosphere of SR2 was six to eight times more than the water-soluble Pb of the bulk soil. SR2 had the highest plant Pb uptake (Table 4) in both sieved and un-sieved soils despite its very low water-soluble Pb in the bulk soil because the plant was able to mobilize Pb in its rhizosphere. This also explains why vegetation did not reduce leaching of Pb in SR2 soils. The grasses in SR2 were probably not able to take up all the Pb mobilized in the rhizosphere and bulk soils. The water soluble Pb of the rhizosphere soils had a positive correlation (p < 0.01, r ¼ 0.58, n ¼ 24) with plant Pb uptake while water-soluble Pb of the bulk soil had no relationship with plant uptake indicating that the plant Pb uptake was from the rhizosphere Pb pool. The rhizosphere watersoluble Pb of SR3 was close to that of the bulk soil in sieved soils suggesting some amount of root exudation. 3.6. Plant Pb uptake and plant biomass of St. Augustine grass Another way to measure bioavailability is through plant uptake
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Table 4 Effect of bullet removal on plant Pb uptake and biomass of St. Augustine grass. SR 1 Shoot
SR 2
SR 3
Root
Shoot
Root
Shoot
Root
1988 ± 364a 2050 ± 292a
580 ± 190a 880 ± 108b
2065 ± 399a 5021 ± 1174b
268 ± 20.5a 252 ± 55a
2068 ± 96.5a 1893 ± 99.5b
174 ± 9.5a 162 ± 7.50a
40 ± 2.46a 59.3 ± 16.7b
194 ± 20.3a 156 ± 14.8b
58.4 ± 3.21a 56.9 ± 4.14a
179 ± 10.6a 159 ± 11.6b
1
Plant Pb uptake (mg kg ) Unsieved 396 ± 71a Sieved 367 ± 109a Plant biomass (g) Unsieved 74.7 ± 6a Sieved 72 ± 5a
Values are means ± standard error, n ¼ 4, .Error includes instrumental error, instrumental drift error, analytical error. SR-shooting range, WAP-weeks after planting, Shoot-aboveground biomass. Treatments followed by same letters are not significantly different at a ¼ 0.05.
since bioavailability has been defined as the proportion of total metals that are available for incorporation into biota which includes plants (John and Leventhal, 1995). The soil pH of vegetated soils was lower than un-vegetated soils in SR1 and SR3 while it was higher in SR2 soils suggesting that the grasses had an acidifying effect in SR1 and SR3. The presence of grasses can increase bioavailability by increasing acidity via processes like root exudation, acidifying effects of CO2 produced in root respiration and Hþ released due to cationic nutrient intake (Levonmaki et al., 2006). Even though plants have mechanisms for increasing metal bioavailability, the high plant Pb uptake recorded in this study showed high bioavailability of Pb in shooting range soils. The plant Pb uptake (Table 4) of St. Augustine grass was comparable and even higher than what is found in the literature. Total plant Pb in grasses ranged from 2145 mg kg1 to 5901 mg kg1 Pb with grasses in SR2 having the highest Pb uptake both in the aboveground (shoots) and belowground (roots) biomass. Pb concentrations in the aboveground biomass ranged from 252 mg kg1 to 880 mg kg1 Pb while root Pb concentrations ranged from 1893 mg kg1 to 5021 mg kg1 Pb. Root Pb concentration of St. Augustine grass was significantly higher than the Pb concentrations in aboveground biomass with about 74e93% of total plant Pb in the roots. Plant roots have the effect of stabilizing Pb in the surrounding soil and Pb retention in the roots is believed to be based on the binding of Pb to ion exchangeable sites on the cell wall and extracellular precipitation (Sharma and Dubey, 2005). Previous studies have reported lower plant Pb concentrations for St. Augustine grass. Cao et al. (2002) reported root concentrations between 110 mg kg1 and 981 mg kg1 and aboveground concentrations between 20 mg kg1 and 77 mg kg1 for St. Augustine grass growing in a battery recycling and salvage yard. Xia (2004) reported even lower concentrations that ranged from 0.44 to 0.66 mg kg1 in roots and 0.41e0.51 mg kg1 for aboveground concentrations of St. Augustine grass growing in a waste dump. St. Augustine grass growing in a metal contaminated site in Florida had 30.8 mg kg1 Pb in the roots and 14 mg kg1 Pb in the above ground biomass (Yoon et al., 2006). Cao et al. (2003b) reported that Pb concentrations in the aboveground biomass was 805 mg kg1 and 1342 mg kg1 in roots of Bermuda grass growing in a shooting range facility. Plant Pb uptake of 1000e1700 mg kg1 was reported by Freitas et al. (2013) in a study where citric acid was used to assist the phytoextraction of Pb by maize and vetiver. St. Augustine took up more Pb without assistance by an acid. The effect of bullet removal on plant uptake had the same trend with that of Mehlich-3 Pb. Sieving had no significant effect in SR1; increased Pb uptake in root and shoot of grasses in SR2; and reduced root Pb uptake of grasses in SR3. The amount of DOC produced may be responsible since bullet removal increased DOC
production. The trend in DOC concentration and plant Pb uptake are the same; SR2 > SR1 > SR3. Plant biomass data (Table 4) showed that St. Augustine grass had higher root biomass in unsieved soils than sieved soils showing a high tolerance to the presence of bullets in the unsieved soil. The grass shows potential to be used in phytostabilization of Pb in contaminated soils. The vegetation of shooting ranges will lead to uptake and immobilization of Pb by plant roots which may help limit contaminant migration, provide ground cover from runoff and help beautify the environment at shooting ranges. 4. Conclusion Bullet removal reduced total soil Pb except in unvegetated SR2; increased bioavailability of Pb in un-vegetated soils; and increased DOC concentration in the leachates. Vegetation reduced leaching of Pb in SR1 and SR3 though a combination of bullet removal and vegetation significantly reduced leaching of Pb in SR2. Vegetation increased water soluble Pb thereby increasing Pb mobility in the soil. The addition of a chemical stabilizer to immobilize Pb may be the solution since vegetation is needed as ground cover. St Augustine grass accumulated high concentrations of Pb by increasing Pb availability in the rhizosphere. A very high proportion of the Pb in the grass was sequestered in the root showing great potentials to be used in phytostabilization of Pb. St Augustine grass had higher plant biomass in unsieved soils with bullets suggesting tolerance to Pb. Further studies may study anti-oxidative responses of St. Augustine grass to Pb toxicity in Pb contaminated soils. Acknowledgement The authors are grateful for the funding assistance from the Florida Department of Environment Protection. References Astrup, T., Boddum, J.K., Christensen, T.H., 1999. Lead distribution and mobility in a soil embankment used as a bullet stop at a shooting range. J. Soil Contam. 8, 653465. Beak, D.G., Basta, N.T., Scheckel, K.G., Traina, S.J., 2006. Bioaccessibility of Pb sequestered to corundum and ferrihydrite in a simulated gastrointestinal system. J. Environ. Qual. 35, 2075e2083. Butler, A., Martin, A., Larson, S., Fabian, G., Nestler, C., 2010. Treatment of metal contaminated soil by the application of lime and grasses. GeoFlorida 2010, 2801e2810. http://dx.doi.org/10.1061/41095(365)285. Cao, X., Ma, L.Q., Chen, M., Satya, P.S., Harris, W.G., 2002. Impacts of phosphate amendments on lead biogeochemistry at a contaminated site. USA. Environ. Sci. Technol. 36 (24), 5296e5304. Cao, R.X., Ma, L.Q., Singh, S.P., Chen, M., Harris, W., 2003a. Phosphate-induced metal immobilization in a contaminated site. Environ. Pollut. 122, 19e28. Cao, X., Ma, L.Q., Chen, M., Hardison, D.W., Harris, W.G., 2003b. Weathering of lead bullets and their environmental effects at outdoor shooting ranges. J. Environ. Qual. 307, 526e534. Chen, M., Daroub, S.H., 2002. Characterization of lead in soils of a rifle/pistol shooting range in central Florida. Soil Sediment Contam. 11 (1), 1e17.
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