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Accumulation of Lead and Arsenic by Carrots Grown on Lead-Arsenate Contaminated Orchard Soils

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  • Chaney Environmental

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Concerns have been raised of possible human food chain transfer of lead and arsenic from crops grown on orchard soils with histories of lead arsenate use. The objective of this study was to determine arsenic and lead uptake by three cultivars of carrots grown on four orchard soils with histories of lead arsenate use. Total concentrations of arsenic and lead in these soils ranged from 93 to 291 and from 350 to 961 mg kg−1 for arsenic and lead, respectively. Arsenic in peeled carrot ranged from 0.38 to 1.64 mg kg−1, while lead ranged from 2.67 to 7.3 mg kg−1 dry weight. This study demonstrated that carrots will accumulate arsenic and lead in the root, which may become a human health risk when consumed. However, further studies are needed to determine what fraction of arsenic and lead in these carrots are bioavailable to humans when consumed.
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Journal of Plant Nutrition, 38:509–525, 2015
ISSN: 0190-4167 print / 1532-4087 online
DOI: 10.1080/01904167.2014.934477
ACCUMULATION OF LEAD AND ARSENIC BY CARROTS GROWN
ON LEAD-ARSENATE CONTAMINATED ORCHARD SOILS
E. E. Codling, R. L. Chaney, and C. E. Green
USDA-ARS, Environmental Management and Byproduct Utilization Laboratory, Beltsville,
Maryland, USA
2Concerns have been raised of possible human food chain transfer of lead and arsenic from
crops grown on orchard soils with histories of lead arsenate use. The objective of this study was to
determine arsenic and lead uptake by three cultivars of carrots grown on four orchard soils with
histories of lead arsenate use. Total concentrations of arsenic and lead in these soils ranged from
93 to 291 and from 350 to 961 mg kg1for arsenic and lead, respectively. Arsenic in peeled carrot
ranged from 0.38 to 1.64 mg kg1, while lead ranged from 2.67 to 7.3 mg kg1dry weight. This
study demonstrated that carrots will accumulate arsenic and lead in the root, which may become a
human health risk when consumed. However, further studies are needed to determine what fraction
of arsenic and lead in these carrots are bioavailable to humans when consumed.
Keywords: orchard, lead-arsenate, carrots, lead, arsenic
INTRODUCTION
Lead arsenate was used as a foliar spray from the 1900s to the1960s
to control codling moth (Cydia pomonella) in apple (Malus sylvestris Mill)
orchards (Merry et al., 1983; Peryea, 1998a). Lead (Pb) and arsenic (As) are
generally immobile in soil and remain in the surface soil due to adsorption by
fine silt and clay particles, amorphous oxides, and organic matter (Merwin
et al., 1994; Peryea, 1991; Renshaw et al., 2006). Accumulated Pb and As
from lead arsenate pesticides are persistent in the environment (Sharma
et al., 2007). Concentrations of Pb and As in some orchards exceeded 900
and 200 mg kg1respectively, (Codling and Ritchie, 2005; Peryea, 1998b).
This article not subject to US copyright law.
Received 18 April 2012; accepted 3 October 2012.
Address correspondence to Eton E. Codling, USDA-ARS, Environmental Management and
Byproduct Utilization Laboratory, 10300 Baltimore Avenue, Beltsville, MD, 20705, USA. E-mail:
eton.codling@ars.usda.gov
509
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510 E. E. Codling et al.
The present study was prompted by the discovery of elevated Pb levels
in commercial carrots sampled by the US Food and Drug Administration in
1998 (Davila, 1999). In their normal market basket food sampling and anal-
ysis program, two carrot samples had anomalous levels of Pb. Both samples,
one from Washington State and the other from Michigan, had been grown
on soils which historically had been used for orchards. Because of food safety
concerns about Pb in carrots, the United State Food and Drug Administra-
tion (US FDA) asked the United States Department of Agriculture (USDA)’s
Agricultural Research Service to investigate the nature of Pb accumulation
in carrots grown on former orchard soils with a history of lead arsenate use.
Lead
Lead is a toxic element that occurs naturally in rocks, soil, plants, wa-
ter, and the atmosphere. Lead has been used in many products such as an
anti-knock compound in gasoline, in pesticides, in paints, and in storage bat-
teries (Peryea, 1998a). It can be harmful to humans when inhaled, ingested
directly through the consumption of contaminated water, or ingested indi-
rectly by consuming crops grown on contaminated soils or irrigated with
contaminated water (Andra et al., 2006; Fewtrell et al., 2004).
Diseases such as neurobehavioral impairment, hypertension, and car-
diovascular disease in humans are attributed to excessive lead exposure,
especially in developing children (Fewtrell et al., 2004). However, plants
generally do not accumulate substantial amounts of Pb in tops or edible
tissues (Chaney and Ryan, 1994). Lead is most available for plant uptake in
soils with low organic matter, low pH, and low phosphate (Zandstra and De
Kryger, 2007). When phosphate is present in the rhizosphere, an insoluble
Pb compound (chloropyromorphite) can be formed near or in the roots
(Cotter-Howells et al., 1999). Brown et al. (2004) reported a reduction in
soluble Pb with increased concentration of phosphate. Nriagu (1978) sug-
gested that Pb in soils with high pH and phosphate will precipitate as lead
phosphate, lead carbonate, or lead hydroxides. All of these processes will
reduce Pb availability for crop uptake.
Studies have shown that some vegetable crops remove Pb from Pb con-
taminated soils. Chisholm (1972) reported that Pb concentration in car-
rots grown on two lead arsenate contaminated soils exceeded the Canadian
residue tolerance levels for human safety of 2 mg kg1. Boon and Soltan-
pour (1992) found that the Pb concentration of leafy vegetables such as
spinach ranged from <5to45mgkg
1when grown on soils with a total
Pb concentration above 2000 mg kg1. Creger and Peryea (1994) concluded
that the increased Pb concentration of leafy vegetable crops grown on a Pb
contaminated soil may have resulted from soil particles containing Pb ad-
hering to the plant surface. Carrot root Pb concentrations reported in the
literature vary widely. Davies and White (1981), for example, observed that
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Lead and Arsenic Uptake by Carrots 511
carrot root Pb concentration ranged from 11–65 mg kg1when plants were
grown on lead contaminated soil having a hot nitric acid extractable Pb level
of 11,620 mg kg1. Jorhem et al. (2000) reported carrot root Pb concentra-
tions ranging from <0.004 to 1.6 mg kg1(fresh weight) in plants grown on
soils with 2 M HNO3extractable Pb ranging from 19 to 265 mg kg1and with
pH ranging from 4.7-5.0, with the highest tissue Pb concentration occurring
at the highest soil Pb concentration and lowest pH.
Arsenic
Arsenic (As) is found naturally in the environment. High exposure to
arsenic has been shown to cause skin, lung and bladder cancer in humans
(Jones, 2007; Ng et al., 2003). Humans can be exposed to As directly through
the consumption of water and indirectly by consuming crops grown on As
contaminated soils or irrigated with contaminated water (Chaturvedi, 2006;
Chen et al., 1992; Diaz et al., 2004; Merwin et al., 1994; Smith et al., 2000;
Zhao et al., 2004). It has been estimated that 35 to 77 million people in
Bangladesh are at risk of As poisoning from drinking As contaminated well
water (Smith et al., 2000). Ahmad et al. (2005) reported that water is the
major pathway for human As contamination. The recommended guideline
set by United States Environmental Protection Agency for As in drinking
water is 10 µgL1(United States Environmental Protection Agency, 1998),
but it currently has no recommended guidelines for As in food crops.
Inorganic arsenite (As III) and arsenate (As V) are the dominant toxic
arsenic species found in food and drinking water (Chaturvedi, 2006; Diaz
et al., 2004). Arsenic is not essential for plant growth and inorganic As
species are generally regarded as potentially phytotoxic when they accumu-
late in soils (Chaturvedi, 2006; Sheppard, 1992). Uptake, accumulation, and
translocation of As by plants is influenced by factors such as 1) soil proper-
ties, 2) soil As concentration, 3) presence of other ions which compete with
As for sorption on soil surfaces, and 4) plant species and age (Chaturvedi,
2006; Jiang and Singh, 1994; Matschullat, 2000). Geng et al. (2006) stated
that soil-plant transfer of As is one pathway for human exposure to As. It is
believed that most food crops are injured by soil As before the crops can ac-
cumulate enough As to become a health risk to humans and animals (Elfving
et al., 1978). For example, Paivoke (1983) observed yield and chlorophyll
reduction in garden pea (Pisum sativum L.) grown hydroponically when As
concentration was 0.7 mg L1, while Jiang and Singh (1994) observed a sig-
nificant yield reduction in barley (Hordeum vulgare L.) when As was applied to
soil at 50 mg kg1either as sodium arsenite or disodium hydrogen arsenate.
Arsenic concentration in plants also varies within crop species. Zandstra and
De Kryger (2007) reported As concentrations of 0.135 mg kg1in peeled
carrot roots grown on orchard soil when total soil As level was 110 mg kg1,
while Elfving et al. (1978) reported As concentration in peeled carrot roots
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512 E. E. Codling et al.
as high as 0.9 mg kg1when plants were grown on a silt loam orchard soil
with 31 mg kg1total As.
Carrots
Carrot is an important fresh market and processing crop that provides
yearly income of over $300 million to US growers. With the conversion of
orchard land to vegetable crop production, there is the potential for planting
carrots on orchard land with a history of lead arsenate use (Preer et al.,
1980; Zandstra and De Kryger, 2007). Therefore, carrot is an economically
important crop to study in relation to lead and arsenic accumulation in
crops.
There are growing concerns that Pb and As will enter the human food
chain when orchards with histories of lead-arsenate use are converted to
vegetable crop production (Merwin et al., 1994). Therefore, the objective of
our study was to evaluate the effect of residual Pb and As in four lead-arsenate
pesticide contaminated orchard soils on yield of and Pb and As uptake by
three cultivars of carrots.
MATERIALS AND METHODS
Collection and Preparation of Lead Arsenate Contaminated
Orchard Soils
Soils were collected from four orchards with histories of lead arsenate
use. The soil series were Bagstown loam (Oxyaquic Hapludults), Spike sandy
loam (Psammentic Haplaquolls), Hudson silty clay loam (Glossaquic Haplu-
dalf ), and Cashmont silt loam (Aridic Haploxerolls). A non-orchard soil, Chris-
tiana fine sandy loam (Typic Paleudult), was collected for use as a control soil.
All soils were adjusted to near pH 6.5 with calcium and magnesium carbonate
and then fertilized with 300 kg ha1of phosphorus (P) as calcium phosphate
[Ca(H2PO4)2] and potassium phosphate (KH2PO4), 100 kg ha1nitrogen
(N) as ammonium nitrate (NH4NO3), 60 kg ha1magnesium (Mg) as mag-
nesium sulfate (MgSO4) and magnesium carbonate (MgCO3) and 232 kg
ha1potassium (K) as KH2PO4. Soil and fertilizers were mixed and incubated
moist (near field capacity) for four weeks.
Experiment
Four kilograms of each soil (based on air dried weight) were placed in 20
×18 cm plastic pots and planted with three cultivars of carrots: ‘Gold King’,
‘Monique’, and ‘Danvers 126’. The cultivars included varieties used for fresh
produce or processing. Soil surfaces of each pot were covered with 2 cm of
plastic beads to reduce splashing during watering. Each soil x carrot cultivar
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Lead and Arsenic Uptake by Carrots 513
was replicated four times. Each pot was placed into a plastic saucer, and pots
were placed in a growth chamber in a randomized complete block design
with 16 hr light at 25Cand8hrdarkat19
C. Plants were watered every
two days or as needed to maintain field capacity. Any leachate collected was
returned to the pots. Eight days after germination, plants were thinned to 5
plants per pot and grown for 90 days.
Carrot tops and roots were harvested. Tops were washed with sodium
lauryl sulfate and rinsed with deionized water. Roots were scrubbed using
a vegetable brush, washed in sodium lauryl sulfate, rinsed multiple times
with de-ionized water to minimize the presence of soil particles in the carrot
peel layer before peeling. Peeled carrot roots, peel, and tops were frozen
at 4C overnight and freeze-dried for 5 days. After yield was determined,
plant tissue was ground using an acid washed mortar and pestle, mixed-well,
and stored until digestion.
Soil and Plant Analysis
Soil pH was measured in a 1:1 soil to water slurry using a combined
electrode; organic carbon was determined with a LECO-CN analyzer (LECO
Corp., St Joseph, MI, USA). Soil texture was determined by the pipette
method (Gee and Bauder, 1986). Total soil As and Pb were determined by
aqua regia digestion (McGrath and Cunliffe, 1985). The Mehlich-3 method
(Mehlich, 1984) was used to determine extractable soil metals and nutrients.
The extracts were analyzed for calcium (Ca), Mg, K, P, manganese (Mn),
copper (Cu), Pb, and zinc (Zn) using a Perkin Elmer inductively coupled
plasma-optical emission spectrometer (ICP-OES) (Perkin Elmer, Waltham,
MA, USA) with scandium as an internal standard. Soil As was determined by
an ICP-OES hydride method outlined by Anderson and Isaacs (1995). The
procedure was as follows: 4 ml of soil extract solution was placed into 15 mL
test tubes and 1.5 mL concentrated hydrochloric acid (HCl; trace element
grade), 2 mL potassium iodide solution, and 2.5 mL 1.73 M sulfamic acid
were mixed and allowed to stand for 30 minutes for reaction to occur. A
0.5% sodium borohydride and 0.05% sodium hydroxide solution was used
to generate arsine gas as it entered the nebulizer of the ICP-OES.
A microwave digestion method as outlined by Codling and Ritchie (2005)
was used for plant sample digestion. Lead and P in the digested solution were
determined using ICP-OES with scandium as an internal standard. Plant
As concentration was determined using the hydride procedure previously
outlined. To ensure accuracy and precision, all samples were analyzed in
duplicate with one blank and one lab standard (peeled carrot root) included
for every ten samples. Peach leaf Standard Reference Material from National
Institute of Standards (NIST-1547, Gaithersburg, MD, USA), was included
after every 30 samples.
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514 E. E. Codling et al.
TABLE 1 Characteristics of the soils before and after pH adjustment. Total metal concentrations for
unadjusted soils are given for Pb and As. After pH adjustment and fertilization, extractable metals and
nutrients of the five soils used in the experiment were determined by Melich-3 extraction
Parameter Christiana Bagstown Hudson Spike Cashmont
texture sandy loam sandy loam silt loam sandy loam silt loam
Before pH adjustment
pH 5.32 5.16 4.49 7.08 5.26
EC ms cm10.48 0.80 1.05 0.35 0.20
OC mg kg118.0 100 43.9 14.4 12.4
As mg kg14.00 133 153 93 291
Pb mg kg120.0 676 435 350 961
Mehlich-3 extraction after pH adjustment
pH 6.29 6.69 6.12 6.07 6.32
As mg kg10.45 20.29 13.15 37.75 110
Pb mg kg1<0.01 263 164 252 524
Ca mg kg1581 2662 2115 1012 1768
Cu mg kg10.63 8.63 5.61 4.79 2.50
Fe mg kg1260 272 359 316 291
Kmgkg
1241 628 247 291 522
Mg mg kg177 287 288 328 333
Mn mg kg19.9 72 35 102 49
Pmgkg
1127 414 201 446 383
Zn mg kg11.70 10.26 0.85 2.60 5.89
Aqua Regia digestion, McGrath and Cunliffe (1985).
In this study, soil and cultivar effects were examined using a factorial
analysis of variance (ANOVA) conducted in a randomized complete block
design. Statistical Analysis System PROC MIXED (SAS Institute, Cary, NC,
USA) was used to model the treatment effects. Means comparisons were
done with Sidak adjusted P-values so that the experiment-wise error was
0.05.
RESULTS AND DISCUSSION
Selected characteristics of soils used in the experiment are presented
in Table 1. The pH of all soils was adjusted to obtain a target pH of about
6.5, which is considered optimum for carrot growth (Sanders, 1998). In the
contaminated soils, total As concentration was 93, 133, 153, and 291 mg kg1
for the Spike, Bagstown, Hudson, and Cashmont soils, respectively, while
total Pb concentration was 350, 435, 676, and 961 mg kg1for the Spike,
Hudson, Bagstown, and Cashmont soils, respectively. As expected, Mehlich-3
extractable As concentrations in the contaminated orchard soils were much
lower than the total concentrations. Total As concentration in these orchard
soils exceeded the 40 mg kg1limit United State Environmental Protection
Agency (USEPA) has set for As contaminated soil (USEPA, 1998). Total Pb
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Lead and Arsenic Uptake by Carrots 515
TABLE 2 Analysis of variance for carrot root
Yield Pb As P
Source DF F-value p-value F-value p-value F-value p-value F-value p-value
Cultivar 2 8.83 0.0023 1.16 0.3462 5.95 0.0259 3.82 0.0514
Soil 4 28.6 0.0001 234 0.0001 97.1 0.0001 2.78 0.0698
Cv ×soil 8 2.05 0.0999 3.16 0.0247 9.05 0.0002 1.39 0.2751
Cv =cultivar.
concentration in three of the four orchard soils exceeded the 400 mg kg1
level considered hazardous to exposed organisms (Dudka and Miller, 1999).
Carrot Yield
Carrot yield was significantly affected at the P<0.05 level by the main
factors soil and cultivar but not by their interaction (Table 2). Carrots grown
on the Bagstown and Hudson soils had the highest dry matter yield, while
carrots grown on the Spike and Cashmont soils yielded less than the control
soil (Figure 1). The higher dry matter yield observed on the Bagstown and
Soils
Carrot Root Yield (g)
0
5
10
15
20
25
30
35
Gold king
Monique
Denver-26
Control Bagstown Hudson Spike Cashmont
FIGURE 1 Carrotroot yield as affected by lead-arsenate contaminated orchard soils. Means plus standard
deviation n =4.
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516 E. E. Codling et al.
Hudson soils compared to the Spike and Cashmont soils may have resulted
from 1) the lower levels of Mehlich-3 extractable soil As, and 2) the higher
levels of organic matter, which sequesters Pb (Brown et al., 2004), in the
Bagstown and Hudson soils (Table 1). Zandstra and De Kryger (2007) re-
ported that lead is most soluble in soils with low organic matter. High levels
of extractable Pb and As have been shown to reduce crop yields (Codling
and Ritchie, 2005; Paivoke, 1983). Comparing cultivars, yield was highest
for ‘Monique’ on all orchard soils but the effect was significant only on the
Bagstown soil (Figure 1). The ‘Monique’ cultivar had larger roots than the
other two cultivars, which contributed to its higher yield.
Elemental Composition of Peeled Carrot Root
Peeled carrot root lead (Pb) concentration was highly significantly af-
fected by soil, slightly affected by the soil ×cultivar interaction, and not
affected by cultivar (Table 2). Peeled carrot root Pb concentration within
carrot cultivar was significantly higher in carrots grown on the lead arse-
nate contaminated orchard soils than in those grown on the control soil
(Table 3). Carrots grown on the Cashmont soil had the highest Pb concen-
tration. The lower Pb concentrations in carrots grown on the Bagstown and
Spike soils may have been the result of higher phosphorus in these soils (Ta-
ble 1). Phosphorus is known to precipitate Pb when applied to lead-arsenate
contaminated orchard soils, making it unavailable for plant uptake (Peryea,
1991). Brown et al. (2004) and Kalbasi et al. (1995) also reported a reduction
in soil soluble lead with addition of phosphate. Although Pb concentration
in peeled carrot roots grown on orchard soils is elevated, it is not clear that
this Pb comprises a risk to consumers. Many human feeding studies with
Pb isotopes have shown that Pb in food is absorbed to a much lower extent
(1–5%) compared to Pb in water (50–80%) (James et al., 1985). The pres-
ence of phytate, fiber, and calcium in foods tends to inhibit Pb absorption,
and the presence of food in the stomach raises the pH, which reduces the
ability of stomach fluids to dissolve Pb from foods or ingested soil. Only one
study has been conducted using Pb incorporated into a food (spinach) fed
to human subjects, and the bioavailability of that Pb was very low (Heard
et al., 1983).
The concentration of arsenic (As) in peeled carrot roots was highly
significantly affected by soil and the soil ×cultivar interaction but only
slightly by cultivar (Table 2). Peeled carrots roots grown on the lead arsenate
contaminated soils had a significantly higher As concentration than did those
grown on the control soil (Table 3). Arsenic concentration in peeled carrot
roots was significantly higher on the Spike and Cashmont soils compared to
the Bagstown and Hudson soils. Mean As concentration was 0.30, 0.40, 1.72,
and1.61mgkg
1for the Bagstown, Hudson, Spike, and Cashmont soils,
respectively. The higher As concentration in carrots grown on the Spike
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TABLE 3 Lead, arsenic and phosphorus concentrations in carrot root grown on four lead arsenate contaminated orchard soils
Pb As P
Gold King Monique Denver 126 Soil mean Gold King Monique Denver 126 Soil mean Gold King Monique Denver 126 Soil mean
mg kg1
Control 0.19dx0.28cx 0.12cx 0.20d§0.05cx 0.04dx 0.06cx 0.05c 2798 2308 2319 2475
Bagstown 2.53cx 2.55bx 2.67bx 2.58c 0.47bx 0.39cx 0.05cy 0.30b 2319 2253 2272 2307
Hudson 3.74x 2.72by 3.55xy 3.34b 0.44bx 0.34cx 0.41bx 0.40b 2350 2225 2075 2217
Spike 2.47cx 2.40bx 2.84bx 2.57c 1.17ay 2.48ax 1.15ay 1.72a 2312 2253 2272 2279
Cashmont 7.23ax 7.11ax 7.12ax 7.15a 1.68abx 1.32bx 1.87ax 1.61a 2313 2182 2202 2233
Cv mean 3.23 3.01 3.26 0.76ab 0.99a 0.69b 2418 2244 2244
Soil means within Cv with different letters (a, b, c, d) are different at the 0.05 significant level.
Cv means within soil with different letters (x, y z) are different at the 0.05 significant levels.
§Soil means with different letters are different at the 0.05 significant levels.
517
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518 E. E. Codling et al.
TABLE 4 Analysis of variance for carrot peel
Pb As P
Source DF F-value p-value F-value p-value F-value p-value
Cultivar 2 3.23 0.066 0.15 0.867 41.1 0.0001
Soil 4 91.3 0.0001 34.6 0.0001 17.2 0.0001
Cv ×soil 8 2.38 0.069 0.12 0.997 4.5 0.0078
Cv =cultivar.
and Cashmont soils may have been due to higher Mehlich-3 extractable As
and P in these soils (Table 1). It has been shown that P application to lead
arsenate contaminated orchard soil increases arsenate solubility making it
more available for crop uptake (Peryea, 1991; Codling, 2007). Carrot As
concentrations in our study were similar to those found by Elfving et al.
(1978) and Zandstra and De Kryger (2007) but higher than those found by
Diaz et al. (2004).
Phosphorus (P) concentration in peeled carrot roots was not significantly
affected by soil, cultivar, or the soil ×cultivar interaction (Table 2). In all
cases, P concentration in peeled carrot roots was within levels considered
sufficient for carrots (Jones et al., 1991; Reuter and Robinson, 1986). There
was no relationship between tissue P concentration and tissue Pb or As
concentration.
Carrot Peel
Carrot peel Pb concentration was highly significantly affected by soil but
not by cultivar or the soil x cultivar interaction (Table 4). Pb concentration
in carrot peel was significantly higher in carrots grown on the lead arsenate
contaminated orchard soils than in those grown on the control soil (Table 5).
Carrots grown on the Cashmont soil had the highest Pb concentration in
the peel followed by those grown on the Spike soil. In all cases, tissue Pb was
higher for peeled carrot roots than for peel (Tables 3 and 5). This result
was unexpected because we initially assumed that soil contamination of the
peel layer was responsible for Pb in root vegetables such as carrots. The high
levels of Pb within peeled carrot roots might be explained by the presence
of xylem vessels that adsorb Pb on their surfaces. Additionally, the formation
of lead phosphates within the xylem may trap Pb in storage roots. Further
studies are needed to verify the form and location of Pb in carrot tissue.
Carrot peel As concentration was highly significantly affected by soil
but not by cultivar or the soil x cultivar interaction (Table 4). Averaged
over cultivars, As concentration in carrot peel was significantly higher in
carrots grown on the orchard soils compared to the result for the control
soil (Table 5). The highest As levels were found in carrot peel grown on
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TABLE 5 Lead, arsenic and phosphorus concentrations in carrot peel grown on four lead arsenate contaminated orchard soils
Pb As P
Gold King Monique Denver 126 Soil mean Gold King Monique Denver 126 Soil mean Gold King Monique Denver 126 Soil mean
mg kg1
Control 0.19 0.13 0.14 0.15c§0.07 0.07 0.07 0.07c 5981ax4929axy 4087ay 4999a
Bagstown 0.74 0.88 0.70 0.77b 0.93 0.92 0.80 0.88b 3990bx 3957axy 3067by 3671b
Hudson 1.27 0.95 0.73 0.98b 0.85 0.74 0.58 0.72b 3787bcx 3474axy 2882by 3382b
Spike 0.91 1.32 1.05 1.09ab 2.09 3.62 2.40 2.71abc 3418cy 3756ax 3273aby 3482b
Cashmont 1.87 1.44 1.29 1.53a 5.48 5.14 5.34 5.32a 3548bcx 3814ax 3155aby 3506b
Cv mean 0.99 0.94 0.78 1.89 2.10 1.84 4145a 3986a 3293b
Soil means within Cv with different letters (a, b, c, d) are different at the 0.05 significant level.
Cv means within soil with different letters (x, y z) are different at the 0.05 significant levels.
§Soil means with different letters are different at the 0.05 significant levels.
519
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520 E. E. Codling et al.
TABLE 6 Analysis of variance for carrot tops
Pb As P
Source DF F-value p-value F-value p-value F-value p-value
Cultivar 2 5.95 0.0259 8.83 0.0023 1.16 0.3462
Soil 4 97.1 0.0001 28.6 0.0001 234 0.0001
Cv ×soil 8 9.05 0.0002 2.05 0.0999 3.16 0.0247
Cv =cultivar.
the Cashmont and Spike soils. The lower As concentration observed in peel
of carrots grown on the Hudson soil reflects the lower level of Mehlich-3
extractable As in this soil (Table 1). Unlike in the case of Pb, As concentration
was higher in carrot peel than in peeled root, with values for carrot peel of
0.88, 0.72, 2.71, and 5.32 mg kg1for the Bagstown, Hudson, Spike, and
Cashmont soils, respectively, compared to values of 0.30, 0.40, 1.72, and
1.61 mg kg1for peeled carrot roots grown on the same soils, respectively
(Tables 3 and 5). The higher levels of As in the peel compared to the
peeled root may have resulted from direct contact between the root and
the lead arsenate contaminated soils, even though the carrots were washed
thoroughly before peeling. Alternatively, the cells of the peel layer may
accumulate As to higher levels than do other carrot cells. Our results are
consistent with those of Helgesen and Larsen (1998), who found that the
As concentration of carrot peel was two to seven times higher than that of
peeled carrot roots. Nevertheless, peeling carrot roots before eating should
not have a substantial effect on the intake of total As due to the low weight
of the carrot peel with respect to the total weight of the carrot (Munoz et al.,
2002).
Carrot peel P concentration was significantly affected by soil, cultivar,
and the soil x cultivar interaction (Table 4). Carrot peel P concentration
was higher on the control soil compared to the lead arsenate contaminated
soils (Table 5). Averaged over soils, carrot peel P was significantly lower in
Danvers-126 compared to the ‘Gold King’ and ‘Monique’ cultivars.
Carrot Tops
The concentration of Pb in carrot tops was highly significantly affected by
soil, cultivar, and the soil ×cultivar interaction (Table 6). Pb concentration
was significantly higher in carrot tops grown on the orchard soils compared
to the control soil (Table 7). As was the case for peeled roots and peel, Pb
concentration in carrot tops was highest on the Cashmont soil, which had the
highest levels of total and extractable soil Pb (Table 1). The extremely high
Pb concentration in tops of the ‘Monique’ cultivar grown on the Cashmont
soil, compared to the other cultivars, resulted in very high variation within
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TABLE 7 Lead, arsenic and phosphorus concentrations in carrot tops grown on four lead arsenate contaminated orchard soils
Pb As P
Gold King Monique Denver 126 Soil mean Gold King Monique Denver 126 Soil mean Gold King Monique Denver 126 Soil mean
mg kg1
Control 0.18cx0.17cx 0.15cx 0.17b§0.09cx 0.07cx 0.11bx 0.09c 4826ax 4387ax 3129ay 4114a
Bagstown 2.23by 3.59ax 2.54abxy 2.79a 1.42bx 1.35bx 2.71bx 1.83b 3582bx 3698ax 2761abx 3347bc
Hudson 2.77abx 2.69ax 3.13ax 2.86a 0.75bx 0.50bcx 1.29bx 0.84b 2688bx 2191bxy 2069by 2316d
Spike 2.35bx 2.80ax 1.8bx 2.32a 5.46ay 5.19abcxy 8.75ax 6.47abc 3429by 4812ax 4032axy 4091ab
Cashmont 4.74ax 9.15abx 2.88abx 5.59ab 5.99ax 4.61ax 8.18ax 6.26a 2838bx 3686ax 2641abx 3055c
Cv Mean 2.45 3.68 2.01 2.74b 2.34ab 4.21a 3473a 3755a 2926b
Soil means within Cv with different letters (a, b, c, d) are different at the 0.05 significant level.
Cv means within soil with different letters (x, y z) are different at the 0.05 significant levels.
§Soil means with different letters are different at the 0.05 significant levels.
521
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522 E. E. Codling et al.
the Cashmont soil treatment, and consequently there was no significant
difference between the Cashmont and control soil means (Table 7). Lead
concentration of carrot tops was similar for the three cultivars when averaged
over soils including the control. In the present study, Pb concentration in
the parts of the carrot plant was in the order peeled carrot root >tops >
peel. These findings disagree with those of Spittler and Feder (1979), who
reported higher Pb concentrations in vegetable tops than in roots.
Arsenic concentration in carrot tops was highly significantly affected
by soil and cultivar but not by the soil x cultivar interaction (Table 6). As
concentration was higher in carrot tops of plants grown on the orchard soils,
compared to results for the control soil (Table 7). Comparing results for the
four orchard soils, As concentration of carrot tops was significantly higher
on the Spike and Cashmont soils, which had higher extractable soil As than
the other two orchard soils. Averaged over soils, As concentration in the
parts of the carrot plant was in the order tops >peel >peeled carrot root.
Similar findings were observed by Elfving et al. (1978) for carrots grown on
a silt loam orchard soil with 31 mg kg1total As.
Carrot top P concentration was significantly affected by soil and the soil
x cultivar interaction (Table 6). Carrot top P was highest in plants grown on
the control and Spike soils (Table 7). Averaged over soils, P concentration
in carrot tops was significantly higher for the ‘Gold King’ and ‘Monique’
cultivars than for Danvers-126. In all cases, P concentration in carrot tops
was at a level that is generally considered sufficient for crop tissue (Jones
et al., 1991).
CONCLUSIONS
This study demonstrated that carrots grown on lead arsenate contami-
nated soils accumulated Pb and As within the edible root, which potentially
could contribute to dietary Pb and As intake by consumers. The concentra-
tion of Pb in the peeled carrot root was higher than in the peel, confirming
that Pb uptake and not just surface contamination contribute to the Pb that
has been found in commercial carrot samples. The Pb concentration in car-
rot tops was also higher than in the peel, though not as high as in the peeled
root, demonstrating that some Pb is translocated from the root to the tops.
Because of the low bioavailability of Pb in food, is not clear that the Pb levels
found in this study comprise a risk to consumers. In contrast to the results
for Pb, As accumulated more in the peel and tops than in the peeled root.
Further studies are needed to determine what fraction of Pb and As in these
carrots would be bioavailable if consumed by humans.
ACKNOWLEDGMENTS
The authors sincerely acknowledge Drs. Darryl Warncke, Wendell
Norvell and Frank Peryea for providing the orchard soils, Dr. Philipp
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Lead and Arsenic Uptake by Carrots 523
Simon, for providing carrots seeds and advice about which carrot cultivars
were commonly grown in the US, and Ms. Mebret Gesese for her technical
assistance in conducting the study.
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Lead (Pb) is a pollutant of a significant public health concern due to its occurrence, persistence and toxicity. Children exposed to high levels of Pb may present serious health problems, such as neurological and adverse developmental effects. In adults, Pb intoxication may also induce severe damages to the central nervous system and even death. The presence of Pb in the environment has several natural and anthropogenic sources. Emissions of Pb have increased drastically, especially after the industrial revolution. A variety of Pb ores has been used to produce additives in gasoline, coal burning, paintings, batteries, electronic goods and other industrial applications. Crops may also be exposed to Pb pollution due to atmospheric deposition; soil and irrigation water contamination; and use of fertilizers and pesticides Pb-containing. This exposition may decrease crop productivity due to Pb toxicity. Previous studies reported that rice is also susceptible to Pb contamination. Under Pb stress, the germination of seeds can be affected, and rice plants may suffer morphological and biochemical damages. Besides the negative effect in plant development, high Pb concentrations (>1000 ng g⁻¹) in rice grains were observed in areas affected by anthropogenic activities such as mining, spill accidents and inappropriate waste disposal. For food safety, it is necessary to keep contaminants within permissible levels. In this sense, many studies have been conducted around the world to verify the nutritional quality of rice, as well as the risks associated with its consumption due to the presence of toxic elements, i.e. lead.
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Increasing soil contamination of arsenic (As) and antimony (Sb) is posing a serious concern to human health. Due to insufficient studies on Sb, the biogeochemical behaviour and plant uptake of Sb are assumed to be similar to that of As. As part of extensive research unravelling As and Sb biogeochemistry and plant uptake, the diffusive gradients in thin films (DGT) technique and sequential extraction procedure (SEP) were applied to evaluate As and Sb uptake by the white icicle radish (Raphanus sativus) cultivated in diluted cattle dip soils contaminated with As only and diluted mining soils contaminated with both As and Sb under agricultural conditions. Labile As and Sb in these soils measured by DGT (CDGT), soil solution (Csol), and SEP (CSEP-labile), were compared with As and Sb bioaccumulation in R. sativus tissues. Regardless of contamination sources and measurement techniques, the results showed that As was consistently more labile than Sb although total As concentrations in two soil types were lower than total Sb. Labile As in cattle dip soils was higher than that in mining soils, although there were no significant differences in soil As concentrations. The analysis of R. sativus tissues revealed that the overall As bioaccumulation was 4.5-fold higher than for Sb, and that As translocation to shoots was limited. In contrast, considerable Sb translocation to shoots was observed. The As and Sb bioaccumulation were strongly correlated with their CSEP-labile, CDGT, and Csol (R2 = 0.87-0.99), demonstrating the effectiveness of these techniques in predicting As and Sb in the white icicle radish. Compared with the cherry bell radish previously studied, the white icicle radish exhibited higher bioaccumulation factors (BAF) for Sb, but lower BAF for As, and lower translocation of As and Sb to shoots, providing understanding of how As and Sb are accumulated by radish cultivars.
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Monoammonium phosphate (MAP) is a popular starter fertilizer in Pacific Northwest tree fruit orchards; however, its use on soils contaminated with lead arsenate pesticide residues can enhance As solubility, thereby increasing As phytoavailability. `Fuji'/EMLA.26 apple trees ( Malus × domestica Borkh.) were planted in Mar. 1992 on a lead arsenate—contaminated Cashmont gravelly sandy loam soil (HCl-extractable soil As range: 60-222 mg·kg ⁻¹ ) using in-hole starter fertilizer application of either MAP or ammonium sulfate at equivalent N and anion rates. In ensuing years, all trees received identical applications of ammonium nitrate only. Relative trunk cross-sectional area was inversely related to soil As concentration in the year of planting but not in subsequent years, and was independent of starter fertilizer treatment. Leaf and fruit As were positively related to soil As in all years. Leaf As was initially higher in the MAP-treated trees; however, this effect diminished over time and disappeared by 1995. Fruit As was independent of starter fertilizer treatment, and was substantially lower than the tolerance established for As in fresh produce. The experimental results indicate that MAP starter fertilizer can increase soil As phytoavailability to apple trees grown under field conditions; however, the effects on tree growth and food safety are insignificant.
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The contamination of groundwater by arsenic in Bangladesh is the largest poisoning of a population in history, with millions of people exposed. This paper describes the history of the discovery of arsenic in drinking-water in Bangladesh and recommends intervention strategies. Tube-wells were installed to provide "pure water" to prevent morbidity and mortality from gastrointestinal disease. The water from the millions of tube-wells that were installed was not tested for arsenic contamination. Studies in other countries where the population has had long-term exposure to arsenic in groundwater indicate that 1 in 10 people who drink water containing 500 mu g of arsenic per litre may ultimately die from cancers caused by arsenic, including lung, bladder and skin cancers. The rapid allocation of funding and prompt expansion of current interventions to address this contamination should be facilitated. The fundamental intervention is the identification and provision of arsenic-free drinking water. Arsenic is rapidly excreted in urine, and for early or mild cases, no specific treatment is required. Community education and participation are essential to ensure that interventions are successful; these should be coupled with follow-up monitoring to confirm that exposure has ended. Taken together with the discovery of arsenic in groundwater in other countries, the experience in Bangladesh shows that groundwater sources throughout the world that are used for drinking-water should be tested for arsenic.
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Total arsenic, selenium, and antimony are determined simultaneously by inductively coupled plasma atomic emission spectrometry (ICP AES) with hydride vapor generation. A1 g wet, 0.25 g dry, or 10 mL water sample is digested by 1 of 2 methods in a 10 mL volumetric culture tube on a programmed heating block by heating with nitric acid and then boiling in a mixture of sulfuric and perchloric acids. For soils, a 0.25 g sample is digested in a 10 mL volumetric culture tube with hydrochloric acid. After digestion, the sample is treated with additional hydrochloric acid. Arsenic, selenium, and antimony are reduced to their hydrides by sodium borohydride in a simplified continuous- flow manifold. A standard pneumatic nebulizer separates the gaseous hydrides (AsH3, SeH2, and SbH3), which are then quantitated by ICP AES at 193.696,196.026, and 231.147 nm, respectively. The detection limits for As, Se, and Sb are 0.55,1.0, and 0.41 μg/L, respectively. Recoveries from 10 matrixes are 65 to 109%; recovery ranges for As, Se, and Sb are 81–109,87–108, and 65–123%, respectively. The method demonstrates good accuracy and precision for environmental samples and is especially suited for analysis of small samples. It requires no additional apparatus for hydride generation or sample introduction.
Article
Potatoes, carrots, beetroots, lettuce and rhubarb were cultivated on soil, that had been severely lead-contaminated by industrial activities at three different locations in Sweden. The vegetables were grown in the gardens of people living in the district, or in some other way making use of the land in the contaminated areas. In some cases, the vegetables were grown in a greenhouse in pots filled with soil from the contaminated sites. Samples of vegetables and soil were collected simultaneously. The vegetables were dry ashed at 450°C and analysed for lead using graphite furnace atomic absorption spectrophotometry with background correction. Certified reference materials were analysed simultaneously with the samples. Soils were extracted according to two methods based on extraction with 2 M HNO3 and NH4OAc, respectively. Lead was determined as above. The pH was determined in a filtered mixture in soil and water (1:2) and recalculated to H+. The results for both vegetables and soils spanned over quite a wide range, for vegetables between < 0.004 and 2.7 mg/kg fresh weight. In the soils, the results ranged from 9.6 to 4400 mg/kg dry weight for the HNO3 fraction, and from 2.3 to 478 mg/kg for the NH4OAc fraction. Regression analysis showed a significant positive correlation (p<0.05) between lead levels in all the vegetables and lead levels in both of the soil fractions together with H+.
Article
Phosphate fertilizer additions to soils containing lead arsenate (LA) pesticide residues can increase As volubility. Apricot (Prunus armeniaca L.) rootstock liners were grown in nondraining pots containing Burch loam soil that received a factorial treatment combination: 1) LA enrichment [no added LA (-LA), and LA added at 138 mg Pb/kg and 50 mg As/kg (+LA)]; 2) fertilizer type [monoammonium phosphate (MAP) and its sulfur analog ammonium hydrogen sulfate (AHS)]; and 3) fertilizer anion rate (0-26.1 mol/m ³ soil). Measured response variables were soil salinity and pH, plant biomass, and plant As and Pb concentrations. Both MAP and AHS increased soil electrical conductivity (EC) and decreased soil pH, with AHS usually being more salinizing and acidifying than MAP was at equivalent rates. Adding LA reduced shoot and root mass and increased As and Pb concentration in shoots and roots. Shoot and root mass were inversely related to soil EC in the -LA soil but not in the +LA soil. Adding MAP increased shoot and root As concentration in the +LA soil, but adding AHS had no effect. Fertilizer type and rate did not influence shoot As concentration or root Pb concentration in the -LA soil or shoot Pb concentration in either the +LA or -LA soil. Adding AHS to the +LA soil increased root Pb concentration. These results are consistent with a P-enhanced solid-phase As release mechanism, which consequently increases plant uptake of soil As. Phosphate amendment had no effect on soil Pb phytoavailability.