arsenic toxicity and accumulation in radish as affected by arsenic chemical speciation
TRANSCRIPT
J. ENVIRON. SCI. HEALTH, B34(4), 661-679 (1999)
ARSENIC TOXICITY AND ACCUMULATION IN RADISH ASAFFECTED BY ARSENIC CHEMICAL SPECIATION
Key Words: Arsenic absorption, arsenic adsorption, arsenic speciation, Rhapanussativus, food contamination
A.A. Carbonell-Barrachina*, F. Burló, E. López and F. Martínez-Sánchez
Departamento de Tecnología Agro-Alimentaria, División Tecnología deAlimentos, Universidad Miguel Hernández, Carretera de Beniel, km 3.2,
03312 Orihuela, Alicante, España/Spain
ABSTRACT
Arsenic (As) uptake by Rhapanus sativus L. (radish), cv. Nueva Orleans,
growing in soil-less culture conditions was studied in relation to the chemical form
and concentration of As. A 4 × 3 factorial experiment was conducted with
treatments consisting of four As chemical forms [As(III), As(V), MMAA, DMAA]
and three As concentrations (1.0, 2.0, and 5.0 mg As L-1). None of the As
treatments were clearly phytotoxic to this radish cultivar. Arsenic phytoavailability
was primarily determined by the As chemical form present in the nutrient solution
and followed the trend DMAA As(V) As(III) << MMAA. Root and shoot As
* Corresponding author, e-mail: [email protected]
661
Copyright © 1999 by Marcel Dekker, Inc. www.dekker.com
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662 CARBONELL-BARRACHINA ET AL.
concentrations significantly increased with increasing As application rates.
Monomethyl arsonic acid treatments caused the highest As accumulation in both
roots and shoots, and this organic arsenical showed a higher uptake rate than the
other As compounds. Inner root As concentrations were, in general, within the
normal range for As contents in food crops but root skin As levels were close or
above the maximum threshold set for As content in edible fruit, crops and
vegetables. The statement that toxicity limits plant As uptake to safe levels was not
confirmed in our study. If radish plants are exposed to a large pulse of As, as
growth on contaminated nutrient solutions, they may accumulate residues which
are unacceptable for animal and human consumption without exhibiting symptoms
of phytotoxicity.
INTRODUCTION
Arsenic (As) has achieved great notoriety because of the toxic properties of
a number of its compounds. Fortunately there are great differences in the toxicity
of different compounds, and the species that are most commonly found in soils are
not the most toxic (O'Neill, 1995). Arsenic differs from many of the common
heavy metals in that the majority of the órgano As compounds are less toxic than
inorganic As compounds after foliar application (Sohrin et al., 1997). However,
residues from the use of organic-based As pesticides and herbicides are more toxic
than inorganic sources (Carbonell-Barrachina et al., 1998).
The major present-day uses of As compounds are as pesticides, wood
preservatives, and as growth promoters for poultry and pigs (O'Neill, 1995). The
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ARSENIC TOXICITY AND ACCUMULATION IN RADISH 663
toxicity of As to biological systems has made it a useful constituent of insecticides,
herbicides, fungicides, and desiccants (Marin, 1995). However, there has been
concern about the build-up of As residues in soils and lake sediments which has
occurred after the use of large quantities of inorganic As compounds which
phytotoxic effects can continue long after application has ceased (O'Neill, 1995).
In Spain, soils where inorganic arsenicals were widely applied are now frequently
used for vegetables growing (Carbonell-Barrachina et al., 1997), including radish.
The bioavailability and uptake of As is dependent on the source, form and
valency of the element (N.A.S., 1977), soil pH, redox and drainage conditions
(Marin et al., 1993), as well as the type and amount of organic matter present
(Mitchell and Barr, 1995). The uptake of As by many terrestrial plants is generally
low so that, even on relatively high As soils, plants do not usually contain
dangerous levels of As; therefore the uptake of As by animals and humans beings
from this source is also low (O'Neill, 1995). Arsenic uptake is also dependent on
plant species, seasonal effects and a number of physical and chemical factors
operating at the soil-root and root-shoot interfaces (Thornton, 1979). Unlike some
marine and fresh water organisms where very high concentrations were found
(similar levels to those in the sediments have been found in some macrophytes), the
levels in terrestrial plants remain well below the level in the soil and the statutory
limit for As in food destined for human consumption, 1 mg As kg"1 fresh weight,
f.w., (Mitchell and Barr, 1995). This suggests that certain plants act as a barrier
between man and toxic concentrations of As in the underlying geological material.
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664 CARBONELL-BARRACHINA ET AL.
In general roots contain higher As levels than stems, leaves or fruit (Lepp,
1981). Translocation of As to the shoots is stopped at the soil-root and root-shoot
interfaces because As is not an essential plant trace nutrient. Although these
interfaces play an important role in controlling the extent of element uptake by
plants, they can be overcome by environmental pressures (Mitchell and Barr,
1995).
The phytotoxic effects of As are indicative of a sudden decrease in water
mobility, as suggested by root plasmolysis and discoloration followed by necrosis
of leaf tips and margins (Machlis, 1941). The sensitivity of a plant to As appears to
be determined by the plant's ability to either not absorb or not translocate the As to
sensitive sites (Mitchell and Barr, 1995). Radish and turnip are amongst the less
sensitive plants to As toxicity (Wauchope, 1983). The degree of uptake and
concentration of As species absorbed from nutrient solutions by turnips plants was
arsenate > arsenite > monomethyl arsonic acid (MMAA) = dimethyl arsinic acid
(DMAA), with toxicity being proportional to the total concentration of As in the
nutrient solution (Guijarro, 1998).
Adherence of contaminated soil particles is a particular problem for root
vegetables, where inadequate washing can lead to the direct ingestion of As
compounds, even if levels in the vegetables themselves are low.
Arsenic can be toxic to radish plants and may accumulate in this plant
species, thereby entering the human food chain. A greenhouse experiment was
designed that allowed the study of As absorption and phytotoxicity to radish plants
in relation to its chemical form. The main objective of this study was to determine
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ARSENIC TOXICITY AND ACCUMULATION IN RADISH 665
whether As could accumulate in the edible-part of radish plants in concentrations
potentially dangerous for human health. The effect of different chemical forms of
As (arsenite, arsenate, MMAA, and DMAA) and three As concentrations (1.0, 2.0,
and 5.0 mg As L"1) on radish plant growth and the distribution of the absorbed As
among root skin, inner root, and shoots is also reported here.
MATERIALS AND METHODS
Radish plants {Rhapanus sativus L.), cv. Nueva Orleans, were grown in
soil-less culture containing different chemical forms and concentrations of As. The
experiment was carried out under greenhouse conditions, using siliceous sand as
inert media for cultivation. The factorial treatments (4 x 3, As species x As
concentrations) were applied in three replicates of a complete randomized design.
The treatments consisted of four chemical forms of As (AsO2~, AsOt, MMAA,
and DMAA) with three As concentrations (1.0, 2.0, and 5.0 mg L'1). Controls with
no added As were also included. The chemical forms of As were added as their
sodium salts. These As levels were selected taking into account that in a previous
study, Carbonell-Barrachina et al. (1997), an arsenite application rate of 2 mg
As(III) L'1 was not phytotoxic to tomato plants, cv. Marmande. Tomato and radish
are both reported as tolerant plant species to As pollution (Wauchope, 1983).
The amount and form of As in solution were analyzed regularly using a
hydride generation atomic absorption technique (Masscheleyn et al., 1991) to
verify that the chemical form of the added As did not change over time. Arsenic
species were found to be stable with respect to oxidation/reduction and
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666 CARBONELL-BARRACHINA ET AL.
methylation/demethylation reactions for a period of 4 days. Thus, the nutrient
solution was replaced every 4 days in order to maintain the desired treatments.
Seeds were germinated in a commercial preparation of peat moss and
vermiculite. Fourteen days after germination, uniform seedlings were selected.
Organic residues were washed from the roots with distilled-deionized water and
seedlings were transferred to hydroponic pots containing 0.5 L of nutrient solution.
A single pot, representing a specific As form — As rate treatment, contained one
seedling. The basal nutrient solution (Feigin et al., 1987) contained (in mg L"1):
126 N; 46.5 P; 136.9 K; 31.6 Mg; 160.5 Ca; 2.0 Fe; 0.8 Mn; 0.3 Mo; 0.5 B; and
0.2 of Zn and Cu. The selection of the P level to be used in this study (46.5 mg P
L"1) was based in two factors: 1) this concentration can be considered as typical of
many fertilized soils where radish is grown (Junta de Extremadura, 1992), and, 2)
it would allow plants to live for a longer period of time than lower P
concentrations (Meharg and Macnair, 1991), though we were aware that a
competition between phosphate and As, mainly as arsenate, could happen and that
the results could be difficult to interpret.
Arsenic treatments started after 14 days of acclimatization. Plants were
grown for 31 days, and then harvested (plants were 59-day old after germination).
Plants were washed with tap water, P-free detergent, and rinsed several times with
distilled-deionized water. Roots and shoots were separated and fresh and dry (60-
70 °C for 72 h) matter productions were determined. Roots were divided in two
parts: root skin and inner root, to distinguish between the adsorption and
absorption processes. Dried samples were ground in a stainless-steel mill to obtain
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ARSENIC TOXICITY AND ACCUMULATION IN RADISH 667
a homogeneous sample. Plant tissue samples were dry-ashed by applying the
methodology of dry mineralization developed by Ybáñez et al. (1992). Digested
samples were filtered and diluted with distilled-deionized water to 25 mL. Arsenic
in the extracts was determined by hydride generation atomic absorption
spectrometry (HGAAS) with a Perkin Elmer (PE) spectrometer Mod. 2100, with a
hydride generator (PE) MHS-10. Acid blanks were analyzed in order to assess
possible As contamination.
Statistical analyses were performed using the PROC ANOVA and PROC
GLM procedures available in SAS (SAS, 1987).
RESULTS AND DISCUSSION
Plant Growth
Radish plants growth (as represented by roots and shoots dry matter
production) was significantly affected by As treatments. Our results demonstrated
that the As chemical form was more important than the As level in solution in
determining the phytotoxic effect of As in this radish cultivar (Table 1). In fact, the
As concentration in the nutrient solution had not statistically significant effects on
plant growth. Arsenic form has been reported as the crucial factor determining As
phytotoxicity in several plants: rice (Marin et al., 1992), Spartina patens and
Spartina alternißora (Carbonell-Barrachina et al., 1998), and tomato (Guijarro,
1998).
Plants treated with arsenate had the highest total root dry matter
production followed by plants treated with MMAA and As(III), though differences
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668 CARBONELL-BARRACHINA ET AL.
TABLE 1
Effects of As Treatments on Dry Matter Production of Radish Plants
ControlAs(III)As(HI)As(m)As(V)As(V)As(V)MMAAMMAAMMAADMAADMAADMAA
Asíate
(mgL-1)
1.02.05.01.02.05.01.02.05.01.02.05.0
Source of variation
As formAs rateAs form x As rate
Source of variation
Arsenic formAs(ni)As(V)MMAADMAA
Arsenic rate1.0 mgL"1
2.0 mgL1
5.0 mg L*1
Root Skin
0.52±0.34f
0.16 ±0.020.28 ± 0.060.32 ±0.090.23 ±0.040.41 ±0.100.37 ±0.060.31 ±0.030.22 ± 0.020.17 ±0.060.22 ± 0.020.20 ± 0.030.13 ±0.03
Dry Matter Production
Inner Root Roots
(RPot1)
0.89 ±0.140.85 ±0.161.77 ±0.631.77 ±0.521.00 ±0.221.98 ±0.541.97 ±0.402.00 ±0.121.47 ±0.311.08 ±0.591.28 ±0.241.70 ±0.160.76 ±0.21
ANOVA F TEST
Root Skin
*t
NSNS
Inner Root
NSNSNS
1.41 ±0.481.01 ±0.182.05 ± 0.682.09 ±0.611.23 ±0.252.39 ±0.642.34 ±0.462.31 ±0.121.69 ±0.331.25 ± 0.651.50 ±0.261.90±0.130.89 ±0.24
Roots
NSNSNS
DUNCAN MULTIPLE RANGE TEST
Root Skin
0.25 ab¥
0.34 a0.23 b0.18 b
0.23 a0.28 a0.25 a
Inner Root
1.46 a1.65 a1.52 a1.25 a
1.28 a1.73 a1.39 a
Roots
1.71a1.99 a1.75 a1.43 a
1.51a2.01a1.64 a
Shoots
0.91 ±0.200.83 ±0.141.59 ±0.331.24 ±0.360.79 ±0.261.33 ±0.271.65 ±0.500.98 ± 0.010.99 ±0.320.73 ±0.291.04 ±0.231.34 ±0.121.70 ±0.39
Shoots
NSNSNS
Shoots
1.22 a1.26 a0.90 a1.36 a
0.91a1.31a1.33 a
t Standard error. JNS = non significant F ratio (p<ß.05), *, **, and •** significant atp < 0.05,0.01, and 0.001, respectively, ^"reatment means from the ANOVA test. Values followed by thesame letter, within the same source of variation, are not significantly different (p<0.05), DuncanMultiple Range Test.
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ARSENIC TOXICrrY AND ACCUMULATION IN RADISH 669
among treatments were not statistically significant; treatments with DMAA caused
similar root dry weights than those of controls. The influence of As concentration
on total root dry production was not significant.
Root skin and inner root dry weights followed a similar pattern, against As,
to that already described for total root dry weight, with DMAA being the most
phytotoxic As form to this plant species.
Arsenic has not been shown to be an essential plant nutrient, although it is
essential for animal metabolism (Lepp, 1981). Stimulation of growth by As
additions (mainly as arsenate) has been, however, reported to increase growth of
maize (Woolson et al. 1971), peas, wheat, potatoes (Jacobs et al., 1970), and rye,
soybean, and cotton (Cooper et al., 1932). It is possible that arsenate additions
may displace phosphate from the soil in certain situations with a resultant increase
in plant-P availability (Jacobs et al., 1970); thereby affecting growth. However, this
speculation cannot be responsible for the increased radish plants dry matter
production of our study because soil-free systems were used.
Marin et al. (1992) also reported an increase in the growth of rice in
hydroponic studies containing DMAA at rates of 0.05 and 0.2 mg As L"1.
Carbonell-Barrachina et al. (1995) reported an increase in tomato plant growth in
nutrient solution containing arsenite at a level of 2.0 mg As L"1 at the first stages of
development. More recently, Carbonell-Barrachina et al. (1998) observed that
applications of arsenate at rates of 0.2 and 0.8 mg L'1 (hydroponic culture)
significantly increased root, shoot and total dry matter production in Sp.
alterniflora and Sp. patens compared to control plants.
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670 CARBONELL-BARRACHINA ET AL.
The reason for the observed positive growth response is unclear, but may
be linked with phosphorus (P) nutrition. Phosphate and arsenate are taken into
plant roots by a common carrier; however, both high and low affinity
phosphate/arsenate plasma membrane carriers have a much higher affinity for
phosphate than arsenate (Meharg and Macnair, 1990). Conversely, Cox (1995),
who studied the effect of different arsenicals on the nutrition of canola plant,
postulated that since As can substitute for P in plant, but is unable to carry out P's
role in energy transfer, the plant reacts as if there is a P deficiency. Thus, as plant
As increases, the plant reacts by increasing P uptake. In this study, there was a
significant interaction between radish plant growth and plant-P, showing that the
growth of this cultivar of radish was dependent on plant-P status. In Figure 1,
radish root skin dry weight has been depicted versus P concentration in root skin
as an example of the "negative" relationship between P and plant growth, implying
that Cox's hypothesis was valid for this plant species.
In this particular experiment, roots- and shoots-P concentrations were
significantly influenced by both As chemical form and As concentration in the
nutrient solution (Table 2). The root skin of plants treated with MMAA presented
significant higher P levels than those of plants treated with inorganic arsenicals and
controls. On the other hand, the highest P concentrations were found in the inner
roots and shoots of plants treated with As(HI) and the lowest P accumulations
corresponded to the organic treatments. While the P concentration in root skin and
shoots decreased with increasing As levels in solution, the inner root P increased.
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ARSENIC TOXICUY AND ACCUMULATION IN RADISH 671
oQ .
S
ü>•535oc
00
ce«
0,5
0,4
0,3
0,2
0,1R =
u0
2- 0.7428; R = 0.5518 ***
2 4 6
Root Skin Phosphorus (g/kg)
• ^ ^
8 1
FIGURE 1Radish root skin dry weight as a function of root skin phosphorus concentration(*** significant at P < 0.001).
Tissue Arsenic Concentration
The total amount of As taken up by radish plants (roots + shoots) followed
the trend: DMAA < As(V) = As(III) « MMAA, with increasing As levels in the
nutrient solution resulting in a higher As uptake for all As species and
concentrations (data not shown; As uptake = As concentration x dry weight). The
highest residues of As are found in plant roots, with intermediate values in the
vegetative top growth, and edible seeds and fruits containing the lowest levels of
As (Lepp, 1981). Upon As absorption, radish plants accumulated As mainly in the
root system; 66.5% of all absorbed As remained in the root system and only 33.5%
reached the shoots.
Berry (1986) suggested three strategies of plant tolerance to metals:
avoidance (limited uptake by roots or limited transport to shoots), detoxification
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672 CARBONELL-BARRACHINA ET AL.
TABLE 2
Effects of As Treatments on P Concentration of Radish Plants
ControlAs(III)Asflll)AsflII)As(V)As(V)As(V)MMAAMMAAMMAADMAADMAADMAA
As rate
(mgL-')
1.02.05.01.02.05.01.02.05.01.02.05.0
Source of variation
As formAs rateAs form x As rate
Source of variation
Arsenic formAs(III)As(V)MMAADMAA
Arsenic rate1.0 mg I/1
2.0 mgL 1
5.0 mgl / 1
Root Skin
8.34±0.01f
5.38 ±0.458.90 ±0.186.11 ±0.035.40 ±0.015.26 ± 0.074.90 ± 0.2510.65 ± 0.266.84 ±0.228.21 ±0.308.52 ± 0.498.60 ± 0.23
Phosphorus
Inner Root
fe kg1)
6.48 ±0.137.38 ± 0.099.15 ±0.099.75 ±0.025.45 ±0.157.19 ±0.368.61 ±0.055.40 ±0.105.54 ±0.015.91 ±0.145.75 ±0.095.44 ±0.14
ANOVA F TEST
Root Skin
***t• * *
***
Inner Root
***
***• * *
DUNCAN MULTIPLE RANGE TEST
Root Skin
6.80 c*5.19 d8.57 a7.94 b
7.49 a7.40 a6.48 b
Inner Root
8.76 a7.08 b5.61c5.52 c
5.99 c6.83 b7.41a
Shoots
6.82 ±0.0910.49 ±0.119.56 ±0.138.18 ±0.126.78 ± 0.066.83 ±0.225.53 ± 0.066.49 ± 0.095.45 ± 0.076.09 ± 0.065.48 ± 0.046.21 ±0.05
Shoots
* • *
* * •
• * *
Shoots
9.41a6.38 b6.01c6.06 c
7.31a7.01b6.58 c
Standard error. *NS = non significant F ratio (p<0.05), *, •*, and **• significant atp < 0.05,0.01, and 0.001, respectively. ^Treatment means from the ANOVA test. Values followed by thesame letter, within the same source of variation, are not significantly different (p<0.05), DuncanMultiple Range Test.
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ARSENIC TOXICITY AND ACCUMULATION IN RADISH 673
(subcellular compartmentalization or by binding to cell walls), and biochemical
tolerance (specialized metabolic pathways and enzymatic adaptations).
When a toxic metal or metalloid has been absorbed by plants, the most
extended mechanism involved in plant tolerance is limiting the upward transport,
resulting in accumulation primarily in the root system (Meharg and Macnair,
1990). From the data on Table 3, it seems that the strategy developed by radish
plants to tolerate the different chemical forms of As was avoidance, limiting As
transport to shoots and increasing As accumulation in the root system. This,
however, does not explain how radish root tissue tolerates such high As
concentrations [up to 69.1 mg As kg'1 on a dry weight basis were found in the root
skin of plants growing in 5 mg MMAA L'1] without exhibiting visual symptoms of
toxicity. A possible explanation, not directly deduced from this study, could be that
As compartmentalization was so effective in radish roots that As impact on growth
and metabolism was minimal. Similar results and hypotheses were reported by
Carbonell-Barrachina et al. (1997) in a study on the influence of arsenite
concentration on As accumulation in tomato and bean plants. Arsenic
detoxification and compartmentalization in root cells are topics that will need
further research to verify their role in plant tolerance to As toxicity.
Besides this As compartmentalization hypothesis there is another factor
that contributed to the low toxicity of As to the radish root system. All the
arsenicals are strongly adsorbed to root surfaces from solution. This adsorption is
apparently limited only by availability. For this reason, observed As concentrations
in roots are very high in hydroponic experiments (Wauchope, 1983), including this
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TABLE 3Effects of As Treatments on As Concentration of Radish Plants, RAI (Root
Absorption Index), and ACR (Tissue As Concentration Ratio)
As rate
(mgL1)
Root Skin Inner Root
Arsenic
Shoots
(mg kg"1)
RAI ACR
ControlAs(ÜI)Asail)As(m)As(V)As(V)As(V)MMAA
AMMAAAMMA
A
ADMAADMAADMAA
1.02.05.01.02.05.01.0
2.0
5.0
1.02.05.0
0.67 ±0.05*24.65 ± 8.2240.94 ± 3.8918.81 ±4.659.46 ± 7.52
21.09 ±6.109.57 ± 0.85
10.90 ± 3.23
51.00 ±4.92
69.10 ±2.4910.36 ± 3.7810.34 ±3.45
0.51 ± 0.127.69 ± 4.048.30 ±0.1411.60 ±1.816.29 ± 5.327.01 ± 1.0815.03 ± 1.75
6.67 ± 1.99
20.86 ±0.35
38.54 ± 1.073.12 ±0.286.73 ±0.38
0.68 ±0.133.68 ± 1.697.81 ± 1.7211.17 ±0.623.67 ±0.923.03 ± 2.0913.78 ±3.87
3.11 ±1.05
11.38 ±1.01
15.42 ± 0.733.15 ±0.457.14 ± 1.52
7.69 ± 4.044.15 ±0.072.21 ±0.366.29 ±5.323.51 ±0.543.01 ±0.35
6.67 ± 1.99
10.43 ±0.18
7.71 ± 0.213.12 ±0.283.37 ±0.19
1.39 ±0.180.55 ±0.040.94 ± 0.221.06 ±0.172.72 ± 1.740.42 ±0.300.99 ± 0.34
0.53 ±0.15
0.55 ±0.05
0.40 ± 0.021.00 ±0.061.07 ±0.24
Source of variation
As formAs rateAs form x As rate
Source of variation
ANOVA F TEST
Root Skin
*•*!
***
In. Root
******• * *
Shoots
NS***
NS
DUNCAN MULTIPLE RANGE TEST
Root Skin In. Root Shoots
RAI
•
NSNS
RAI
ACR
NSNSNS
ACR
Arsenic form
As(V)MMAADMAA
Arsenic rate1.0 mgL1
2.0 mgL1
5.0 mg L '
22.65 b¥
10.18 c41.60 a12.94 c
7.89 b26.14 a31.50 a
9.01b9.45 b
22.02 a8.56 b
5.94 c10.73 b20.11a
7.61a6.83 a9.97 a9.29 a
3.44 c7.34 b14.48 a
4.68 b4.27 b8.27 a3.22 b
5.94 a5.36 a4.02 a
0.85 a1.38 a0.49 a1.07 a
1.20 a0.78 a0.90 a
1 Standard error. *NS = non significant F ratio (p<0.05), *, **, and •** significant at p < 0.05,0.01, and 0.001, respectively. *Treatment means from the ANOVA test. Values followed by thesame letter, within the same source of variation, are not significantly difierent (p<0.05), DuncanMultiple Range Test.
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ARSENIC TOXICITY AND ACCUMULATION IN RADISH 675
study. Our results clearly demonstrated that there is a significant difference
between As concentrations caused by adsorption (root skin) and those caused by
absorption (inner root), with the highest levels being due to adsorption onto the
root surfaces.
In general, As concentrations in roots significantly increased with
increasing As levels in the nutrient solution. The data on the root absorption index
(RAI = root As concentration / nutrient solution As level) seemed to indicate that
the chemical form of As present in the nutrient solution mainly determined the
phytoavailability of As to radish plants. Arsenic phytoavailability followed the
trend: DMAA <, As(V) <, As(III) « MMAA. The higher the As level in the
nutrient solution, the higher the As concentrations in roots and shoots.
The As addition rate had a significant effect on shoot As level; As
concentration in shoot tissue increased significantly with increasing As levels in the
nutrient solution. Tissue As levels found in shoots were lower than those found in
the root system, especially in the root skin. Shoot As concentrations were also
influenced by the As chemical form. Similarly to the As accumulation pattern in
root as affected by the As chemical form, MMAA caused the highest As
accumulations in shoots, though results were not statistically different.
The tissue As concentration ratio (ACR = shoot As concentration / inner
root As concentration) was not significantly affected by either As chemical form or
As application rate.
The data on tissue As concentration indicated that the As chemical form
present in the nutrient solution and the application rate not only determined the
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676 CARBONELL-BARRACHINA ET AL.
phytoavailability of As to radish plants but also determined the transport and
movement of As in the plant. Treatments with both organic arsenicals caused
higher As levels in shoots than those caused by inorganic compounds. This study,
therefore, has also shown that MMAA and DMAA, usually thought of as contact
herbicides (Wauchope, 1983), are also quite active via root entry and xylem
transport.
Arsenic levels in vegetables, grain, and other food crops at the consumer
level are low, and have decreased in last three decades (Jelinek and Corneliussen,
1977). The usual statement (e.g., Lepp, 1981) that toxicity limits plant As uptake
to safe levels was not, however, confirmed in our study. Under conditions of
exposure to threshold levels in the soil, the statement appears to be true. If,
however, crops are exposed to a large pulse of As, as growth on contaminated
nutrient solutions, they may accumulate residues which are unacceptable for human
consumption. These high As concentrations found in plant tissues of soil-less
culture studies are likely due to the fact that As concentrations in the nutrient
solutions are not high enough to cause plant death but are high enough to make
plants absorb As continuously leading to very high levels of pollutant.
The limit set for As content in ftuit, crops and vegetables is 1.0 mg kg'1
f.w. (Mitchell and Barr, 1995); considering an average water content of the edible
part of the radish plants in our experiment of 95%, this limit on a dry weight (d.w.)
basis is 20 mg kg"1. In our study, As concentration in the skin of radish roots were
in some plants close or even above this maximum threshold and ranged from 9.5 to
69.1 mg kg'1 (d.w.). These high As concentrations are, without a doubt, a result of
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ARSENIC TOXICITY AND ACCUMULATION IN RADISH 677
all the arsenicals being firmly adhered to the root surfaces from solution
(Wauchope, 1983). Arsenic concentrations in the inner roots were, however, lower
than those of the root skins and ranged from 3.1 to 38.5 mg kg'1 (d.w.), but, in
some cases, they were still above this statutory limit. Therefore and taking into
account a possible incorporation of As in the food chain, soil residues from the use
of As-based pesticides and herbicides are potentially dangerous for the human
health due to their feasibility of accumulating high levels of As in the edible part of
radishes and even more if these radishes are consumed with peelings because of the
As adsorption to the root surface.
CONCLUSION
The statement that toxicity limits plant As uptake to safe levels was not
confirmed in our study. If radish plants are exposed to a large pulse of As, as
growth on contaminated nutrient solutions, they may accumulate residues which
are unacceptable for animal and human consumption without exhibiting symptoms
of phytotoxicity or growth reduction. Arsenic concentrations in the root skin were
statistically higher than those of the inner root likely due to arsenicals being firmly
adhered to the root surfaces, and, in general, both concentrations were clearly
above the maximum statutory limit for As in food destined for human
consumption.
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