Professional Documents
Culture Documents
DOI 10.1007/s00244-012-9867-z
Abstract The purpose of this study was to investigate the Brazil, India, and Mexico) have considerably large areas
availability of the heavy metals cadmium (Cd), lead (Pb), with a deficiency of this element (Alloway 2008). More-
and chromium (Cr) to soil and maize plants fertilized with over, most of the major annual crops, such as corn, rice,
different sources and doses of zinc (Zn) in a Rhodic bean, and soybean, have expressive sensitivity to Zn defi-
Eutrudox soil. For that purpose, concentrations of Cd, Pb, ciency (Alloway 2009).
and Cr were evaluated in leaf tissue and grains of maize This fact increases fertilizer consumption in each crop
plants and in 0–20 and 20–40 cm soil layers after fertil- year. During the 1960s, approximately 46 million tons of
ization with four doses of Zn from eight different sources fertilizers were used, and in 2030 it was estimated that
of fertilizer. There was no accumulation of Cd, Pb, and Cr 157.3 million tons of them will be necessary for crops
in maize grain and Cd and Cr in leaf tissue of the plants; throughout the world (Ayoub 1999; Daher 2008). Fur-
nevertheless, there was accumulation of Pb in leaf tissue, thermore, according to Yamada (2004), micronutrient
showing its availability throughout different sources of Zn consumption in Brazil increased 13.3 times in the period
and consequent uptake by plants. Regarding the soil, it was from 1990 to 2003.
observed that fertilizer from the different sources made Cd, This high and growing dependence on fertilizer to
Pb, and Cr available at increasing amounts proportional to achieve greater crop yields raises concern from an envi-
increased Zn doses. Under experimental conditions, fertil- ronmental perspective because the fertilizers used to supply
ization with Zn increased concentrations of heavy metals both macronutrients and micronutrients may have heavy
Cd, Pb and Cr in soil, further highlighting the importance metals in their composition in addition to the desirable
of conducting more studies related to the application of elements (Gonçalves Junior et al. 2000). This fact becomes
mineral fertilizers for micronutrient supply and the avail- even more significant in developing countries, such as
ability of heavy metals. Brazil, where in general legislation and monitoring are less
strict compared with those of developed countries. In other
developing countries, e.g., Argentina, there have also been
Micronutrient deficiency and consequent provision of reports of heavy-metal contamination problems in agri-
micronutrients occur ever more frequently in agricultural culture, (Gimeno-Garcı́a et al. 1996; Camelo et al. 1997)
crops throughout the world (Gimeno-Garcı́a et al. 1996; and China (Zhuang et al. 2009; Jan et al. 2010; Yang et al.
Accioly et al. 2000; Oliveira et al. 2001). Among micro- 2011). Elements such as cadmium (Cd), lead (Pb), and
nutrients used in agriculture, zinc (Zn) stands out because chromium (Cd), may accumulate in soil and be taken up by
major grain-producing countries (i.e. United States, China, plants, thus leading to contamination of the environment,
the food chain, and underground waters, resulting in seri-
ous environmental damage (Usman & Mohamed 2009;
H. Nacke (&) A. C. Gonçalves Jr D. Schwantes Baldantoni et al. 2010).
I. A. Nava L. Strey G. F. Coelho
In recent years, with a view toward decreasing costs in
Western Paraná State University, Pernambuco Street 1777,
Marechal Cândido Rondon 85960-000, Brazil fertilizer production in Brazil, some companies that for-
e-mail: herbertnacke@hotmail.com mulate these products have been using industrial residues
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Arch Environ Contam Toxicol
as a source of nutrients, which often proves to be dangerous A randomized block experimental design was used in
because, in addition to desirable micronutrients, these this experiment in an 8 9 4 factorial arrangement with
sources may contain toxic elements (Rodella 2005; Gon- three replications, with the factors being constituted by
çalves Junior et al. 2011). Moreover, there are signs that eight different sources and four different doses of Zn (0, 2,
some of the formulators of micronutrients have been 4 and 6 kg ha-1) for a total of 32 treatments and 96
importing industrial waste from developed countries and experimental plots. The eight sources of Zn used in this
using it as raw material in producing their fertilizers experiment were in the form of granules from seven fer-
(Gonçalves Junior & Pessoa 2002), a practice considered tilizer companies that used two raw materials, zinc oxide
illegal according to the Basel Convention established in (ZnO) and another called ‘‘fritted trace elements’’ (FTE),
1992 by the United Nations Environment Program. which are micronutrients bonded with silicates at high
Based on the situation indicated described previously, a temperatures. Because this work aimed to evaluate the
study was undertaken for the purpose of evaluating the fertilizers available on the market, all sources were pur-
availability of the heavy metals Cd, Pb and Cr to soil and chased commercially so that we would have only the
maize plants (Zea mays L.) fertilized with different sources producers’ information about the origin and formulation of
and doses of the micronutrient Zn in a Rhodic Eutrudox their product. Thus, the sources were classified in the fol-
soil in the setting of a field experiment. lowing manner:
Source A = granulated ZnO with 15 % Zn from com-
Experimental pany 1
Source B = granulated ZnO with 10 % Zn from com-
The experiment was performed in the municipality of Mer- pany 2
cedes, PR, Brazil (248 41’ S and 548 25’ W (Fig. 1); average Source C = granulated FTE with15 % Zn from com-
altitude 415 m). The climate of the location is subtropical pany 3
(Cfa) according to Köppen classification, without a defined Source D = granulated FTE with 15 % Zn from com-
dry season and with hot summers and a tendency for con- pany 4
centrated rainfalls during this season. The annual average Source E = granulated FTE with 10 % Zn from com-
temperature of the region is 21 °C (minimum of 14 °C, pany 5
maximum of 28 °C). The soil in the experimental location is Source F = granulated FTE with 15 % Zn from com-
classified as Rhodic Eutrudox (Food and Agriculture Orga- pany 6
nization 2006) and has a clayey texture (558.50 g kg-1 clay, Source G = granulated ZnO with 2 % Zn from company
278.61 g kg-1 silt, and 162.89 g kg-1 sand). 1 (but with a different formulation)
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Arch Environ Contam Toxicol
Source H = granulated FTE with 15 % Zn from com- had been planted for 2 years with a soybean–maize
pany 7 succession.
At 25 days after emergence (DAE), top dress fertilization
It should be emphasized that in this study only the
was performed for the N nutrient with the application of
doses of Zn were varied so that fertilization with
100 kg ha-1 N in the form of urea (Coelho 2006). To
macronutrients—which were applied at the time of sowing
determine the bioavailability of Cd, Pb, and Cr to maize
and consisted of the elements nitrogen (N), phosphorus
plants, contents of these elements in leaf tissue and kernels
(P), and potassium (K)—was identical in all of the treat-
were determined using nitric perchloric digestion (Associ-
ments. As macronutrient sources, ammonium sulfate
ation of Analytical Communities 2005) followed by FAAS
[(NH4)2SO4] was used for N; simple super-phosphate (SS)
(Welz & Sperling 1999). For this purpose, leaf tissue was
was used for P; and potassium chloride (KCl) was used
collected on the appearance of female inflorescence (stage
for K.
R1) (Ritchie et al. 2003) i.e. at 61 DAE. Leaves from the part
Table 1 lists the following: concentrations of Cd, Pb,
opposite and below the upper ear of four plants, which were
and Cr at depths of 0–20 and 20–40 cm of the soil used in
chosen randomly from each plot, were collected, placed in
the experiment as well as the Zn sources and the prepared
clean bags, and identified. In the laboratory, leaves were
N:P2O5:K2O fertilizer formulation. To obtain these data, all
washed with detergent and distilled, deionized water;
materials were ground and homogenized to a particle
afterward, the midrib of the leaves was removed and the
size \2 mm, after that nitric perchloric digestion (Associ-
leaves dried in a forced-air circulation laboratory oven at 65
ation of Analytical Communities 2005) was performed,
°C for 48 h. Then the leaves were ground, homogenized to a
followed by flame atomic absorption spectrometry tech-
particle size \2 mm, stored in clean bags, and identified for
niques (FAAS) (Welz & Sperling 1999).
later analysis.
Each evaluation plot of the experiment consisted of five
Maize kernels were collected at 119 DAE at the end of
planted rows at a spacing of 0.9 m width and 4.0 m length.
the experiment, at which time collection of the ears from
The three center rows were used as the useful plot, ignoring
the entire useable plot was performed. After the kernels
the 1.0 m border at the edges, thus yielding a useable area
were dried, they were ground and homogenized to a par-
of 5.4 m2. The area in which this experiment was per-
ticle size \2 mm, stored in clean polyethylene bags, and
formed was managed by a conventional planting system
identified for later analysis.
without the practice of turning the soil; however, this area
In addition, after the end of the experiment, soil samples
were collected to study the availability of Cd, Pb, and Cr
from different sources of Zn. For that purpose, three soil
Table 1 Concentrations of Cd, Pb, and Cr in experimental soil at
samples were collected at a depth of 0–20 cm within each
depths of 0–20 and 20–40 cm from eight Zn fertilizer sources as well
as in the prepared N:P2O5:K2O mixture as well as maximum allow- experimental plot using a Dutch auger. The samples were
able values by Brazilian legislation mixed to form a single compound sample. The same pro-
Sample Cd Pb Cr cedure was performed to obtain samples from the
(mg kg-1) (mg kg-1) (mg kg-1) 20–40 cm layer of the soil. After soil samples were col-
lected, they were sent to the laboratory and dried in a
Soil (0–20 cm) 1.03 25.32 10.29
forced-air circulation laboratory oven at 40 °C for 48 h.
Soil (20–40 cm) 1.22 34.83 10.97 The samples were ground, stored in clean polyethylene
Source A 178.89 2,746.82 309.87 bags, and identified for later analysis using nitric perchloric
Source B 245.06 2,450.57 20.28 digestion (Association of Analytical Communities 2005)
Source C 123.37 1,362.55 33.14 followed by FAAS (Welz & Sperling 1999).
Source D 203.82 9,872.82 1,304.42 For statistical analysis of the data, GENES software
Source E 237.19 2,011.39 33.21 (Cruz 2006) was used with analysis of variance (ANOVA)
Source F 115.08 1,380.96 27.62 at the 5 % significance level first being performed. If there
Source G 6.54 233.47 48.56 was a significant effect among the sources, Tukey test at
Source H 211.74 11,039.46 1,347.45 5 % probability was used; for the Zn doses, polynomial
N:P2O5:K2O 3.67 32.12 14.68 regression analysis was used. For the purpose of adjusting
Maximum allowable valuea 450.00 10,000.00 NAb for normality of the data, transformation of the data for leaf
a
Maximum allowable value for Cd and Pb in fertilizers based on concentrations of Pb, Cd and Cr in the 0–20 cm soil layer
normative instruction no. 27 from the Brazilian ministry of agricul- and of Cr in the 20–40 cm soil layer was necessary. The
ture, livestock and food supply (Brazil 2006) root square transformation of the sum of the value of the
b
There is no maximum allowable value for Cr result at 0.5 was used.
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Arch Environ Contam Toxicol
Results and Discussion compared with the other sources. These results may be
explained by the Pb concentrations in these two sources
We compared the concentrations of Cd and Pb obtained (Table 1), which were greater than that of the other sour-
from the analysis of the fertilizers with the maximum ces. Moreover, regarding leaf Pb concentrations in the
values permitted in fertilizers for supply of micronutrients breakdown of the interaction among doses and sources of
as stipulated by the Brazilian Ministry of Agriculture, Zn, a linear effect (P \ 0.05) was obtained only for sources
Livestock and Food Supply by means of Normative D and H (Fig. 2). The maize plants were not saturated with
Instruction No. 27 of 2006 (Table 1). The allowable Pb, showing that maize plants may naturally accumulate
maximum values of Pb and Cd are 10,000.00 and greater quantities of this metal and that sources D and H
450.00 mg kg-1, respectively, but only fertilizer from provided effective Pb availability to the crop.
source H contained greater Pb levels (11,039.46 mg kg-1). The greatest dose of Zn used in this experiment
It should be noted that in this Normative Instruction, which (6.0 kg ha-1) provided 7.87 and 7.27 mg kg-1 of Pb from
is the current guideline for fertilizer inspection in Brazil, sources D and H, respectively, showing that a critical
reference values are not presented for Cr concentrations in concentrations of Pb (10 mg kg-1) did not occur in the
fertilizers for micronutrient supply, which may permit the plants. Nevertheless, these values may be considered high
use of residues with high concentration of this heavy metal. because they occurred with only one application of fertil-
In the chemical analyses undertaken in this study, Cd izer from these Zn sources.
and Cr contents were not detected in leaf tissue of plants, These results show that more studies related to mineral
and Cd, Pb, and Cr were not detected in maize kernels. fertilization with micronutrients and contamination by
According to (Kabata-Pendias and Pendias 2001), the heavy metals are necessary because continuous application
maximum level of Cd in agricultural crops is may lead to greater accumulations of these elements in the
0.05–0.5 mg kg-1; the maximum level of Cr is 5 mg kg-1; soil and thus increase their consequent availability to plants
and the maximum level of Pb is 0.5–10 mg kg-1. The lack (Camelo et al. 1997).
of detection of these metals in our soils may be considered Regarding Cd concentrations in the two soil layers
normal because the plants may take up significant quanti- evaluated, a growing linear increase (P \ 0.05) of this ele-
ties of heavy metals such as Cd, Pb and Cr; however, these ment was observed as a function of Zn dose (Figs. 3 and 4).
metals in general are not greatly translocated to cereal The greatest dose of Zn used in this experiment
grains (Mortvedt 2001; Malavolta 2006; Shtangeeva et al. (6.0 kg ha-1) made an average of 2.27 and of 2.76 mg kg-1
2011). It should be noted that this dynamic generally of Cd available to the soil in the 0–20 and 20–40 cm layers,
occurs in soils with low concentrations of heavy metals; in respectively.
soils with high concentrations, plants may accumulate According to Resolution 420 of the Brazilian National
these elements in their grains. Dudka et al. (1994) studied Environmental Council (CONAMA) (Brazil 2009), which
wheat development in soils with high concentrations of Cd establishes soil-quality guidelines regarding the presence
and observed that this toxic heavy metal did not prove to be of chemical substances in Brazil, the maximum value
harmful to plants; however, the grain produced by them permitted in agricultural areas is 3 mg kg-1. The greatest
had levels considered toxic for animals and human beings. Cd concentrations obtained in this study were less than,
Analysis of variance (ANOVA; Table 2) showed that albeit near, the maximum limit permitted by Brazilian
for leaf Pb concentrations, there was a significant differ- legislation.
ence (P \ 0.05) for the sources and doses of Zn as well as Moreover, comparing Cd values obtained in soil samples
the interaction between these two factors. Cd and Cr con- with (1) maximum values commonly found in soils of the
centrations in the 0–20 cm soil layer and Cd and Pb con- United States (2.00 mg kg-1) and Russia (1.14 mg kg-1)
centrations in the 20–40 cm soil layer showed a significant (Kabata-Pendias and Pendias 2001), (2) values normally
difference (P \ 0.05) only for Zn dose. For Pb concen- found in soils (0.01 to 2.00 mg kg-1) (Bowen 1979), and (3)
trations in the 0- to 20-cm soil layer, a significant effect the limit value established by the environmental quality
was observed (P \ 0.05) for Zn dose as well as the inter- standards of China (State Environmental Protection
action between source and dose of Zn. Finally, for Cr Administration 1995 [0.60 mg kg-1]), it may be inferred
contents in the 20- to 40-cm soil layer, there was no sig- that the Zn sources used in this experiment made Cd
nificant difference (P [ 0.05) among any of the factors available to the soil at a contaminant level.
evaluated. Regarding Pb concentrations in soil after the experi-
Mean values of Pb concentrations in leaf tissue of maize ment, for the 0- to 20-cm layer in the breakdown of sig-
plants are listed in Table 3, where it may be observed that nificant interaction, an effect was only obtained for sources
the D and H sources of Zn provided greater contents D and H, just as was observed for leaf Pb. Thus, regression
(P \ 0.05) of this toxic heavy metal to leaf tissue of plants was performed for these sources, in which we determined
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Arch Environ Contam Toxicol
Table 2 ANOVA for the results of Pb concentrations in leaf tissue of maize plants as well as Cd, Pb, and Cr concentrations in 0–20 cm and
20–40 cm soil layers
VS df Mean squares
Leaf Pb Cd Pb Cr Cd Pb Cr
0–20 cm 0–20 cm 0–20 cm 20–40 cm 20–40 cm 20–40 cm
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Arch Environ Contam Toxicol
16
2 [Cd] = 0.249x + 1.262
R² = 0.867 [Cr] = 1.359x + 10.632
14 R² = 0.892
12
1 10
0 2 4 6 0 2 4 6
Fig. 4 Cd concentration in the 20–40 cm soil layer as a function of Fig. 7 Cr concentration in the 0–20 cm soil layer as a function of Zn
Zn dose dose
50
limit stipulated for agricultural soils (72 mg kg-1). In the
Source D Source H case of Pb, it should be highlighted that values of this
Soil Pb concentration (mg kg-1)
Source D Source H
Source D
element in soil at the dose of 0 kg ha-1 Zn, which corre-
45
[Pb] = 3.174x + 27.491 sponds to Pb content in experimental soil without appli-
R² = 0.989
cation of Zn, ranged from 27.56 to 36.53 mg kg-1 for the
40
0–20 cm and 20–40 cm soil layers, respectively, showing
Source H that the soil already had a high initial content of this toxic
35
[Pb] = 2.915x + 26.733
R² = 0.998
heavy metal, probably from fertilizers applied before this
study.
30
Pb contents in both soil layers were greater than
the average of farmable soils in the United States
25
0 2 4 6 (10.6 mg kg-1), Poland (20.9 mg kg-1), and worldwide
Zn doses (kg ha-1) (25 mg kg-1) (Kabata-Pendias & Pendias 2001), within the
levels commonly found in soils (2–300 mg kg-1) (Bowen
Fig. 5 Pb concentration in the 0–20 cm soil layer as a function of the
D and H doses of Zn used in the experiment
1979), and lower than the environmental quality standards of
China (350 mg kg-1 [State Environmental Protection
Administration 1995]).
55
For Cr, regression was performed only for the 0–20 cm
Soil Pb concentration (mg kg-1)
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Arch Environ Contam Toxicol
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Arch Environ Contam Toxicol
in agriculture. CNPq, FAPESP, POTAFOS, Jaboticabal, Brazil, State Environmental Protection Administration (1995) Environmental
p 237 quality standard for soils. SEPA, Beijing, China
Oliveira IP, Kluthcouski J, Santos RSM, Fancelli AL, Dourado Neto Usman ARA, Mohamed HM (2009) Effect of microbial inoculation
D, Faria CD (2001) Residual concentration of cupper, iron, and EDTA on the uptake and translocation of heavy metal by
manganese and zinc in a RHODIC eutrudox under different soil corn and sunflower. Chemosphere 76:893–899
managements. Pesq Agropec Trop 31:97–103 Varjabedian R, Leite CBB (2009) Office 1029/2009 – PGJ/CAO.
Paula Junior D (2011) Office 2147/09-MP-PJCS-UMA. Available Available at: http://www.mma.gov.br/port/conama/processos/FE
at: http://www.mma.gov.br/port/conama/processos/FE4582B1/Of 4582B1/ConsideracoesMinisPublSaoPaulo.pdf. Accessed: May
2147-09-MP-PJCS-UMA_7maio09.pdf. Accessed May 15, 2012 15, 2012
Rauret G (1998) Extraction procedures for the determination of heavy Welz B, Sperling M (1999) Atomic absorption spectrometry (2nd ed).
metals in contaminated soil and sediment. Talanta 46:449–455 Wiley-VCH, Weinheim
Ritchie SW, Hanway JJ, Benson GO (2003) How the corn plant Yamada T (2004) Micronutrient deficiencies, occurrence, detection
develops. POTAFOS, Piracicaba, Brazil and correction: The Brazilian experience success. POTAFOS,
Rodella AA (2005) Regulation of contaminant contents in fertiliz- Piracicaba, Brazil
ers—a case study. Rev Bras Ci Solo 29:797–801 Yang Q, Xu Y, Liu S, He J, Long F (2011) Concentration and
Ryser P, Sauder WR (2006) Effects of heavy-metal-contaminated soil potential health risk of heavy metals in market vegetables in
on growth, phenology and biomass turnover of Hieracium Chongqing, China. Ecotoxicol Environ Saf 74:1664–1669
piloselloides. Environ Pollut 140:52–61 Zhuang P, Mcbride MB, Xia H, Li N, Li Z (2009) Health risk from
Shtangeeva I, Steinnes E, Lierhagen S (2011) Macronutrients and heavy metals via consumption of food crops in the vicinity of
trace elements in rye and wheat: Similarities and differences in Dabaoshan mine, South China. Sci Total Environ 407:1551–1561
uptake and relationships between elements. Environ Exp Bot
70:259–265
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