Acta Scientiarum

http://www.uem.br/acta
ISSN printed: 1679-9275
ISSN on-line: 1807-8621
Doi: 10.4025/actasciagron.v36i1.17539

Reducing conditions on barium absorption in rice plants cultured in

BaSO4-enriched soil
Marcio Osvaldo Lima Magalhães1*, Nelson Moura Brasil do Amaral Sobrinho1, Everaldo Zonta1,
Alfredo Tolón Becerra2, Xavier Bolívar Lastra-Bravo2 and Izabella Bezerra Coutinho1
1
Departamento de Solos, Universidade Federal Rural do Rio de Janeiro, BR-465, km 7, 23890-000, Seropédica, Rio de Janeiro, Brazil. 2Rural
Engineering Department, University of Almería, Almería, Spain. *Author for correspondence. E-mail: [email protected]

ABSTRACT. To evaluate the possible solubilization of barium sulfate in soils under reducing conditions
and its effects on barium bioavailability, an Oryza sativa pot trial was established. Increasing barium doses
and two redox potential conditions were evaluated. The geochemical fractionation data demonstrated that
reducing conditions led to an increase in the levels of more labile forms of barium and a reduction in more
stable forms. Furthermore, higher doses of barium were found to have a negative impact on grain
production. The highest levels of barium accumulation in the leaves, roots, and grains were observed with
the highest barium dose under reducing conditions. These results demonstrate that reducing conditions
increased barium bioavailability and absorption by rice plants.
Keywords: contamination, barite, Oryza sativa.

Efeito do potencial redox na absorção de bário por plantas de arroz cultivadas em solos
enriquecidos com BaSO4
RESUMO. Com o objetivo de avaliar a possível solubilização do sulfato de bário em solos sob condições
redutoras e aumento da biodisponibilidade do bário, instalou-se ensaio em vasos com Oryza sativa.
Avaliaram-se doses de bário e duas condições de potencial redox. Os resultados do fracionamento
geoquímico demonstraram que a condição de redução favoreceu o aumento nos teores de bário nas formas
de maior labilidade e diminuição nas formas de maior estabilidade. A produção de grãos foi influenciada, de
forma negativa, pela aplicação da maior dose de bário. Os teores mais elevados e acúmulo de bário nas
folhas, raízes, e grãos foram encontrados na maior dose e na condição de redução. Esses resultados
evidenciaram que a condição de redução proporcionou maior biodisponibilidade desse elemento.
Palavras-chave: contaminação, baritina, Oryza sativa.

Introduction that trigger a series of physical, chemical, and

biological transformations. These changes
Barium is present in small quantities in igneous
rocks such as feldspars and micas. The primary subsequently produce soil characteristics that are
source, however, is the mineral barite (BaSO4), profoundly distinct from the initial conditions
which is widely used in the petroleum industry as a (SEYBOLD et al., 2002). These new chemical
drilling fluid component due to its high density environments are ecologically relevant because the
(4.2 g cm-3) (FAM et al., 2003). Barite (BaSO4) often change redox states affecting the mobility and
is added as a weighting agent to drilling muds to bioavailability of elements present in the soil.
counteract pressure in the geologic formations being The barium contained in barite is relatively
drilled, preventing a blowout (NEFF, 2008). During immobile, and its low water solubility (2.47 mg L-1
the drilling of oil wells for oil prospecting and at 25°C) reduces its bioavailability. However, the
production, the drilling fluid is mixed with ground solubility of barium sulfate can be improved under
rock, thus releasing its component substances highly reducing environments (MAGALHÃES
(POZEBON et al., 2005). Consequently, these et al., 2011a; MONNIN et al., 2001), reflecting the
component substances greatly influence the fact that sulfate reduction occurs at Eh values of
concentration of barium and other substances in oil -250 mV (KHANAL; HUANG, 2003). Previous
well residues (MELTON et al., 2000). studies have shown that barite can serve as a sulfate
Soils in flood areas exhibit alterations in source for the respiration of anaerobic bacteria
elemental composition and microbial metabolism (BALDI et al., 1996). When these wastes are
Acta Scientiarum. Agronomy Maringá, v. 36, n. 1, p. 119-127, Jan.-Mar., 2014
120 Magalhães et al.

disposed into poorly drained soil, the release of the saturated soil until stabilization of the redox
most toxic form of barium, Ba+2, into the potential required for the reduction of sulfate was
environment (USEPA, 2005) may contaminate obtained (i.e., Eh values of -250 mV). The Eh values
bodies of water and introduce the element into the of the soil under oxidizing and reducing conditions
food chain (MAGALHÃES et al., 2011b). were directly measured using a specific electrode.
Because barium is present in most soils, low, Combined ORP analyzer electrodes were used for
non-toxic levels of barium, approximately 4 to measuring Eh, and half-cell pH analyzer electrodes
50 mg kg-1, are commonly found in plants were used for measuring pH with the pH/Ion
(CHAUDHRY et al., 1977). Nogueira et al. (2010), 450M® Analyzer. Thirty days after a redox potential
for example, found no signs of barium toxicity in value of -250 mV was obtained, rice seedlings (Oryza
corn plants with barium concentrations ranging sativa var. Bico Ganga) were transplanted to the pots.
from 90 to 106 mg kg-1. In a hydroponic trial The choice for rice was due to the fact that it is a
conducted with soy plants, however, Suwa et al. culture that adapts to both dryland and flooding
(2008) observed signs of toxicity, namely, high conditions.
concentrations of barium in the leaves (4,970 mg kg-1) Following the incubation period, the barium was
and reductions in dry mass, following treatment geochemically fractionated for all experimental
with 5 mM barium. treatments according to the method recommended
The aim of the present study was to test the by the European Communities Bureau of Reference
effects of oxidizing and reducing conditions on the (BCR) and adopted by Sahuquillo et al. (1999). The
bioavailability of barium and its absorption by rice geochemical fractions were as follows: the acid-
plants (Oryza sativa). soluble fraction, extracted with 0.11 mol L-1 acetic
acid (F1); the fraction bound to Fe and Mn oxides,
Material and methods extracted with 0.1 mol L-1 hydroxylamine
hydrochloride (F2); the fraction bound to organic
The soil samples used were collected from an matter, extracted with 8.8 mol L-1 hydrogen
Oxisol, at a depth of 0-20 cm, in the State of Rio de peroxide and 1.0 mol L-1 ammonium acetate (F3);
Janeiro, Brazil. The soil characteristics were as and the residual fraction, which represents the aqua
follows: barium: 223 mg kg-1 (ISO, 1995), pH in regia extracts from all other fractions (F4).
H2O: 5.8; sand: 272 g kg-1; silt: 132 g kg-1; clay: 596 g Ten days after germination, seedlings
kg-1; Corg.: 10,7 g kg-1 and a CEC(pH 7.0): 97.0 mmolc homogeneous in size and vigor were selected, and
dm-3 (EMBRAPA, 1997). two plants were transplanted into each pot. A
Using barium sulfate (BaSO4) as a source, parceled fertilization method was used, with 80 kg
barium doses were applied according to the values N ha-1, 40 kg P ha-1 (single dose), and 40 kg K ha-1
proposed by the 420 CONAMA Resolution applied at the time of planting. After 40 days, surface
(BRASIL, 2009). The treatments were as follows: fertilization was performed by applying 40 kg N ha-1
soil without barium application (control); 100 mg and 40 kg K ha-1. The plants were collected at the
barium kg-1 of dry soil (dose 1); 300 mg barium kg-1 end of the experiment, after approximately 4 months
of dry soil (dose 2); and 3,000 mg barium kg-1 of dry of growth, corresponding to the growth cycle of the
soil (dose 3). cultivar. The collected plants were separated into
The pots were filled with 5 dm3 of soil, and the shoots, roots, and grains and then rinsed in
soil was homogenized after the barium doses were deionized water. The plant samples were oven-dried
added. The moisture conditions were 70% of field at 70°C until a constant weight was obtained. The
capacity (oxidizing conditions) and saturation digestion material was obtained by grinding the
(reducing conditions). To maintain the reducing shoots, roots, and grains in a Willey-type mill using
conditions, a 7 cm layer of water was applied to the a 2 mm mesh. Nitroperchloric digestion was used to
soil surface. During the incubation period, drainage determine the barium concentrations, at a ratio of
was impeded for all treatments, and the pots were 6:1, according to the method described by Tedesco
covered to prevent water loss by evaporation. A total et al. (1995). The total barium content in the shoots,
of 32 experimental units were prepared in a factorial roots, and grains were calculated using the
design (4 x 2) with four barium levels, two moisture determined concentration and the amount of dry
levels, and four replicates. matter produced.
During the incubation period, pH and Eh values The levels of barium in the soil and plant extracts
were determined 2 hours after flooding on days 2, 4, were quantified using a plasma emission
and 6. Following the first week of incubation, the spectrometer (ICP-OES; Perkin Elmer, model
assessment was performed on a weekly basis for the OPTIMA 3000), with Detection Limit = 0.036 mg kg-1
Acta Scientiarum. Agronomy Maringá, v. 36, n. 1, p. 119-127, Jan.-Mar., 2014
Reducing conditions on barium absorption 121

and Quantification Limit = 0.36 mg kg-1 for barium. pH values in the present study indicate that the
To validate the determination of the pseudo total incubation period was sufficient to promote these
content of barium in the soil and plants, the conditions and thus favored the reduction of
following reference materials were used: NIST oxidized soil components, particularly sulfate.
SRM 2709a (San Joaquin soil) and SRM 1573a
(tomato leaves), which had barium concentrations of
979 ± 28 mg kg-1 (95% recovery) and 63 mg kg-1
(93% recovery), respectively. These values are
within the range classified as normal by the National
Institute of Standards and Technology (NIST) for
soil and plant samples. The oxidation-reduction
variations were assessed by analysis of variance with
F-test (ρ < 0.05), and the mean values of soil redox
potential conditions compared by Tukey test
(ρ < 0.05). Analyses were performed using the
SAS/STAT 9.2® software (SAS Institute Inc., Cary,
NC, USA). An error bar was also used to highlight
possible differences among barium contents for the
same redox potential condition.

Results and discussion

Figure 1A shows that the soil Eh values at 70%
field capacity ranged from ± 350 to 450 mV, which
is within the range for oxidized soil (800-300 mV)
(CAMARGO et al., 2001). The pH values also
remained constant, ranging from 5.8 to 6.0. When
saturation conditions in the soil were combined
with prolonged flooding (Figure 1B), a reduction in
Eh values and subsequent stabilization below
-250 mV were observed, indicative of highly
Figure 1. Redox potential values (Eh) for two condidition
reducing conditions. According to the literature (oxidized and reduced) and the relationship between Eh and pH
(KHANAL; HUANG, 2003; JONES; INGLE JR., after weeks of flooding.
2005; MAGALHÃES et al., 2011b), the reduction of
sulfate to sulfide by sulfate-reducing bacteria (SRB) Figure 2 shows the mean barium distributions in
in the soil may occur at this Eh value. At the onset of the different geochemical fractions obtained by BCR
flooding, Eh values of -250 mV and pH values scheme. Shows that under reducing conditions in
below 6 were observed. As saturation continued, Eh the soil (-250 mV), the barium concentration in the
values decreased, and pH values increased until acid soluble fraction (F1) increased significantly.
stabilizing at an approximately neutral value. The increases observed for the different treatments
The observed increase in pH is characteristic of under reducing conditions were as follows: 11 mg kg-1
soils under flooding conditions and reflects the for the control, 25 mg kg-1 for dose 1, 87 mg kg-1 for
accumulation of protons (GONÇALVES et al., 2008; dose 2, and 135 mg kg-1 for dose 3. Higher treatment
LIMA et al., 2005; VEPRASKAS; FAULKNER, 2001). doses yielded greater increases in the barium
As described by Seybold et al. (2002), Eh and pH levels concentration of the F1 fraction. This fraction
reflect the activity of protons and electrons in the soil contains barium in solution that is electrostatically
because the excess of one causes a deficit in the other. adsorbed on the surface of the soil colloids
According to Camargo et al. (1999), the increase in pH (exchangeable) and precipitated in the form of
after submergence depends not only on the ratio of carbonates (FILGUEIRAS et al., 2004; MARIN
OH- and H+ consumption but also on the ratio of H+ et al., 1997).
and electron consumption. The change in pH The increased barium concentration in the F1
necessarily depends on two conditions: a well- fraction under saturated conditions was accompanied
developed reduction process and a sufficient by decreased barium concentrations in the oxide-
amount of reduced Fe (SEYBOLD et al., 2002; bound (F2) and residual (F4) fractions. The binding
PONNAMPERUMA, 1978). The measured Eh and of heavy metals with oxides does not guarantee
Acta Scientiarum. Agronomy Maringá, v. 36, n. 1, p. 119-127, Jan.-Mar., 2014
122 Magalhães et al.

surface immobilization because these elements can be For both of the redox potential conditions, no
released by oxide reduction in this fraction, resulting significant differences were observed in the shoot,
in a negative impact on the soil biota (CHLOPECKA, root, and total dry matter production of control
1996; RODRIGUEZ et al., 2009). No significant plants and rice plants treated with arying barium
differences were observed for the barium doses (Figure 3). However, differences in grain mass
concentration in the organic matter fraction (F3). were observed in plants that received the highest
These results demonstrate the low affinity of barium barium dose and plants without BaSO4 application
for organic matter, because this complex is considered (control). Relative to the control, the highest barium
limited by some authors (BODEK et al., 1988; dose resulted in decreases of approximately 18% and
DANG et al., 2002). Used geochemical fractionation 38% in grain yield under oxidizing and reducing
and observed that only 1% of the total barium was conditions, respectively. The findings of the present
present in the fraction bound to organic matter study therefore indicate that the highest barium dose
(SMEDA; ZYRNICKI, 2002). The results of the (3,000 mg kg-1) negatively affected grain yield. In the
geochemical fractionation in the present study literature, there is limited information about the
demonstrate that reducing conditions increased influence of barium on plant metabolism. However,
barium concentrations in the most labile fraction (F1) in a study that utilized Glycine max in a nutrient
and reduced the amount of barium associated with solution, Suwa et al. (2008) reported similar results:
more stable fractions (F2 and F4). The increase high barium doses affected plant development,
observed in F1, which was promoted by increased particularly yield, demonstrating the phytotoxic
BaSO4 solubility, may result in increased barium effect of this element. Llugany et al. (2000) observed
bioavailability (ALBERTA ENVIRONMENT, 2009; phytotoxicity symptoms in Phaseolus vulgaris plants
MAGALHÃES et al., 2011b). even at low barium concentrations.

Figure 2. Barium distribution in different geochemical fractions as a function of dose and redox potential (oxidized and reduced). F1:
soluble acid fraction; F2: fraction bound to iron and manganese oxide; F3: fraction bound to organic matter and sulfides; F4: residual
fraction. Letters (for each barium content) indicate a significant difference (p < 0.05). Control: no barium sulfate application; Dose 1: 100
mg kg-1; Dose 2: 300 mg kg-1; Dose 3: 3,000 mg kg-1.

Acta Scientiarum. Agronomy Maringá, v. 36, n. 1, p. 119-127, Jan.-Mar., 2014

Reducing conditions on barium absorption 123

Figure 3. Dry mass production of rice plants as a function of barium dose and redox potential (oxidized and reduced). Letters (for each
barium content) indicate a significant difference (p < 0.05). Control: no barium sulfate application; Dose 1: 100 mg kg-1; Dose 2: 300 mg
kg-1; Dose 3: 3,000 mg kg-1.

In the present study, the biomass of rice plants Among the different doses treatments, no
was significantly different under the two soil redox significant differences in barium content were
conditions, with a greater biomass observed in observed in the shoots of rice plants cultivated in
reduced soils than in oxidized soils. Although oxidized soil (Figure 4), and the mean concentration
reducing conditions yielded greater grain mass at all was 180 mg kg-1. However, there were differences in
doses, this increase was lowest at the highest dose, barium absorption by rice plants under reducing
and significant differences were observed between conditions, with the lowest concentrations observed in
doses. the control (150 mg kg-1) and the highest
There is no reference data describing the toxicity concentrations (620 mg kg-1, approximately 4 times
of barium to rice plants grown in nutrient solution. higher) observed in plants that received the highest
Although there are no reports of the effects caused barium dose (dose 3). The effects of doses 1 and 2 were
by the toxicity of barium, they may be associated to not significantly different. A comparison of the barium
the deficiency of other elements due to competition, content on plant shoots under different redox potential
for instance, competition with calcium for root revealed no significant differences in the control
absorption, due to its similarity (NOGUEIRA et al., (background levels of barium). For plants treated with
2010). BaSO4, however, reducing conditions resulted in the
According to the data obtained, higher highest barium concentrations. At the highest dose,
moisture levels (saturation) resulted in higher dry reducing conditions resulted in a 3-fold increase in the
matter production for all of the evaluated barium content of plant shoots. Absorption in plant
parameters. Thus, saturation positively influenced roots was also dependent on the dose under both soil
the development of plants. Several studies have redox conditions. The following barium
shown that the highest rice yields are obtained concentrations were measured in plants cultivated in
under flood conditions. For example, Patel et al. oxidized soil: 61 mg kg-1 for the control, 222 mg kg-1
(2010) observed a mean reduction of 27% in plant for dose 1, 508 mg kg-1 for dose 2, and 826 mg kg-1 for
yield when plants were cultivated under oxidizing dose 3. There was a 13-fold increase in the barium
conditions compared to flooded cultivation concentration in plants that received the highest dose
(reducing conditions). compared to the control. Furthermore, the significant
Acta Scientiarum. Agronomy Maringá, v. 36, n. 1, p. 119-127, Jan.-Mar., 2014
124 Magalhães et al.

differences observed in reduced soil were greater than values of barium absorption they observed in Zea
those in oxidized soil. Under reducing conditions, mays plants ranged from 90 to 106 mg kg-1. These
there was a 36-fold difference between the control and levels were not found to influence plant development
the highest dose. Analysis of the barium content in the or produce toxicity symptoms. In a Glycine max
grains revealed higher concentrations in plants cultured hydroponic trial, Suwa et al. (2008) observed high
under reducing conditions compared to oxidizing concentrations of barium in the leaves (4,970 mg kg-1)
conditions, especially at higher doses. following a treatment dose of 5 mM barium. These
levels led to decreased dry mass production, which is
one indicator of phytotoxicity.
Another trend observed in the present study was
increased translocation of barium from the roots to
the leaves under low dosage concentrations. In
contrast, higher barium concentrations in the soil
(doses 2 and 3) decreased translocation, resulting in
greater barium immobilization in the roots. The
ability of plants to immobilize metal in the roots is
one of the mechanisms some plant species have
evolved to tolerate heavy metals present in the soil
(MAGALHÃES et al., 2011a; SANTOS et al., 2007).
The first barrier against the entering of heavy
metals, especially regarding root level, is the
immobilization of heavy metals in the cell wall and
by extracellular carbohydrates, such as mucilage and
callose (FRITZ, 2007; KARTEL et al., 1999),
avoiding the presence of free ions in root tissues
and, consequently, the translocation of ions to
shoots, thereby reducing phytotoxicity. Pectins and
histidine stand out for immobilizing heavy metals in
the cell wall (LEITA et al., 1996).
Among the doses treatments, no significant
differences were observed with respect to the amount
of barium accumulated in the shoots and grains under
oxidizing conditions (Figure 5). Under reducing
conditions, however, plants cultured at the highest
dose exhibited greater accumulation relative to the
control. In the roots, there was a significant difference
between the control and the dose treatments for both
redox potential. An assessment of the total barium
accumulated in the roots under oxidizing conditions
revealed that the only significant difference was
between the highest dose and the control. Under
reducing conditions, the effect for the highest dose was
significantly different from all other dosage treatments
and the control. For natural concentrations of barium
Figure 4. Barium concentration in leaves, roots, and grains of in the soil (control), there was no significant difference
rice plants as a function of barium dose and redox potential in barium accumulation as a function of redox
(oxidized and reduced). Letters (for each barium content) conditions (oxidized and reduced). For the dose
indicate a significant difference (p < 0.05). Control: no barium treatments, however, reducing conditions resulted in
sulfate application; Dose 1: 100 mg kg-1; Dose 2: 300 mg kg-1;
Dose 3: 3,000 mg kg-1. higher barium accumulation, except in the roots,
where a significant difference was only observed at the
The levels of barium that can be considered highest dose. The accumulation increase in plants
normal or toxic for plants are not well established grown under reducing conditions was approximately
(SUWA et al., 2008). According to Nogueira et al. 3-fold for the shoots, roots, filled grains, and
(2010), barium is commonly found in plant tissues accumulated total at the highest dose. Except in the
but not at levels that can be considered toxic, and the control, differences were observed in the amount of
Acta Scientiarum. Agronomy Maringá, v. 36, n. 1, p. 119-127, Jan.-Mar., 2014
Reducing conditions on barium absorption 125

accumulated barium between the two soil redox approximately 40% of the maximal value of barium.
conditions, with greater accumulation observed under This value may be considered high because barium is
reducing conditions. found in many food groups and in water (USEPA
These findings demonstrate that highly reducing 2005; YSART et al., 1999). It is also important to
conditions improve barium sulfate solubility. As compare the values obtained in this study with the
demonstrated by the geochemical fractionation (Figure values measured in plants grown in soil with natural
2), barium bioavailability increased, enabling barium concentrations (control). Under such
absorption and accumulation of this element in plants. conditions, the daily ingestion of barium from rice
It is worth noting that the increase in barium would be 1.8 mg, or 13% of the reference dose.
accumulation in the grains was approximately 300%, Pearson correlation analysis was performed for the
this increases the probability of introducing barium barium extracted in the acid soluble fraction (F1) and
in to the food chain because rice grains are a staple the barium absorbed and accumulated in different
food in many countries. plant parts for the two redox potential conditions
According to the United Nations Food and (Table 1). High and significant correlations were
Agriculture Organization, the consumption of rice observed for all variables, except for barium
around the world amounts to an average 84.8 kg concentration and accumulation in the grains under
person-1 year-1, which is equivalent to an average daily oxidizing conditions. The correlation of the barium
consumption per person of approximately 230 g. The concentration in F1 with barium concentration in the
maximum daily ingestion of barium per kg of body leaves under reducing conditions was greater (r = 0.87)
mass suggested by the United States Environmental than the correlation under oxidizing conditions
Protection Agency (USEPA, 2005) is 0.2 mg kg-1 bw (r = 0.54). A similar pattern was observed in the roots,
day-1. Based on this information, a person weighing with the highest correlation always under reducing
70 kg may ingest a maximum of 14 mg of barium per conditions. There was no correlation between the
day. If this person consumes an average of 230 g day-1 barium concentration in F1 and the concentration and
of rice grains produced under the most critical accumulation of barium in the grains under oxidizing
conditions presented in this study (extremely reduced conditions. However, a high correlation (r = 0.86) was
soil with the highest amount of barium), this person observed for these parameters under reducing
would ingest a total of 5.5 mg of barium, or conditions.

Figure 5. Barium uptake in leaves, roots, grains, and whole rice plants as a function of barium dose and redox potential (oxidized and
reduced). Letters (for each barium content) indicate a significant difference (p < 0.05). Control: no barium sulfate application; Dose 1:
100 mg kg-1; Dose 2: 300 mg kg-1; Dose 3: 3,000 mg kg-1.

Acta Scientiarum. Agronomy Maringá, v. 36, n. 1, p. 119-127, Jan.-Mar., 2014

126 Magalhães et al.

In general, higher correlations were observed Micronutrientes e elementos tóxicos na agricultura.

under reducing conditions than under oxidizing São Paulo: Potafós, 2001. p. 89-117.
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higher levels of barium found in the F1 fraction Barium toxicity in plants. Communications in Soil
Science and Plant Analysis, v. 8, n. 9, p. 795-797,
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RINCON, J. Heavy metal distribution and chemical Creative Commons Attribution License, which permits unrestricted use, distribution,
speciation in tailings and soils around a Pb–Zn mine in and reproduction in any medium, provided the original work is properly cited.

Acta Scientiarum. Agronomy Maringá, v. 36, n. 1, p. 119-127, Jan.-Mar., 2014