Published in J. Environ. Qual. 32:2216-2222 (2003).
© ASA, CSSA, SSSA
677 S. Segoe Rd., Madison, WI 53711 USA
TECHNICAL REPORTS
Organic Compounds in the Environment
Behavior of 14C-Atrazine in Argentinean Topsoils under Different Cropping Managements
S. Hang*,a,
E. Barriusob and
S. Houotb
a University of Córdoba, CC 509, 5000 Córdoba, Argentina
b National Institute of Agronomical Research, Environment and Arable Crops, BP 01, 78850 Thiverval-Grignon, France
* Corresponding author (shang{at}agro.uncor.edu).
Received for publication December 12, 2002.
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ABSTRACT
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Atrazine (6-chloro-N2–ethyl-N4–isopropyl-1,3,5-triazine-2,4-diamine) behavior was studied in four surface soils during incubations in laboratory conditions. Soils were chosen in relation to their cropping management (tillage and no tillage) and crop rotation system (continuous soybean [Glycine max (L.) Merr.] and maize (Zea mays L.)–soybean rotation). A natural soil under brushwood was sampled as a reference. Atrazine use in field conditions was associated with maize cropping, thus only one soil received atrazine every other year. Atrazine behavior was characterized through the balance of 14C-U-ring atrazine radioactivity among the mineralized fraction, the extractable fraction, and the nonextractable bound residues. Soil organic matter capacity to form bound residues was characterized using soil size fractionation. Accelerated atrazine mineralization was only observed in the soil receiving atrazine in field conditions. Atrazine application every other year was enough to develop a microflora adapted to triazine ring mineralization. Bound residue formation was rapid and increased with soil organic matter content. The coarsest soil size fractions (2000–200 and 200–50 µm) containing the nonhumified organic matter presented the highest capacity to form bound residues. No effect of tillage system was observed, probably because of the uniform sampling depth at 20 cm, hiding the stratification pattern of soil organic matter in nontilled soils.
Abbreviations: OC, organic carbon • SOM, soil organic matter • TMA, total microbial activity
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INTRODUCTION
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IN ARGENTINA atrazine is the second-most sold herbicide (Secretaría de Agricultura, Ganadería, Pesca y Alimentos, 2001), due to an increase in the applied doses. Chemical, physical, and biological properties of soil affect its persistence (Koskinen and Clay, 1997). Temperature, water content, oxygen status, soil type, atrazine concentration, crop and soil management are the determining factors of its half-life (Topp et al., 1995; Stolpe and Shea, 1995; Di et al., 1998). Depending on the interactions between these factors, half-life value may vary extensively from less than one week to more than one year (Weber, 1991; Koskinen and Clay, 1997; Vanderheyden et al., 1997). Organic matter is the main component regulating atrazine behavior in soils (Houot et al., 1997). In addition to the total content of soil organic matter (SOM), its distribution between fresh and humified organic matter influences atrazine retention (Barriuso and Koskinen, 1996). Soil organic matter plays a dual role in affecting atrazine sorption and microbial activity responsible for pesticide degradation (Di et al., 1998).
Soil tillage management may influence the interactions between herbicide and soil by modifying the total content of SOM and its characteristics (Locke and Bryson, 1997). No-tillage generally results in an increase in SOM, depending on the previous soil management and cropping sequence (Martens, 2001). In soils under no-tillage management, the proportion of nonhumified SOM usually increases as compared with soils under conventional tillage (Andriulo et al., 2000; Murdock et al., 2000). The tillage system may also induce changes in the composition of soil microbial community (Abril, 2002). The clearing of trees and brushwood from virgin soils and the immediate use of these soils for agriculture under no-tillage systems is an increasing practice in Argentina. These recently cropped soils present a higher proportion of nonhumified organic matter than soils with several years of agriculture, and SOM decrease due to agricultural activity is mainly related to SOM loss from nonhumified fractions larger than 100 µm (Quiroga et al., 1999).
Atrazine is a herbicide mainly used for maize crop treatment. Thus, the frequency of maize in the crop succession determines the frequency of atrazine use. The possible adaptation of soil microflora to atrazine degradation due to its frequent use on the same soil has been demonstrated, resulting in accelerated degradation of the herbicide and percentages of mineralization reaching up to 60% of the atrazine applied (Barriuso and Houot, 1996).
The aims of this study were to assess the effect of soil tillage management and crop succession on the behavior of 14C-atrazine in topsoils of Argentinean semiarid pampa. The behavior of 14C-atrazine was studied in laboratory incubations by following the distribution of radioactivity between mineralized, extractable, and nonextractable residues. The importance of SOM humification in the formation of nonextractable residues was assessed using soil size fractionation.
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MATERIALS AND METHODS
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Soils
The upper horizon (0–20 cm) of four soils classified as Molisolls according to Soil Survey Staff (1998) were sampled in December 2000, in the semiarid pampa of the province of Cordoba, Argentina (Fig. 1)
. Three soils were selected based on their different tillage management (no tillage and conventional tillage), crop succession (continuous soybean and soybean–maize rotation), and frequency of atrazine use as described in Table 1. An additional soil was sampled under natural brushwood as native control.
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Fig. 1. Location of sample sites in the province of Córdoba, Argentina. S1, No-tillage with field atrazine application; S2, no-tillage without field atrazine application; S3, conventional tillage without field atrazine application; and S4, brushwood without field atrazine application.
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After sampling, the soils were air-dried and sieved to 2 mm. Particle size distribution among sand, silt, and clay fractions was done by sieving and sedimentation. The soil pH was determined in water (soil to water, 1:1) and organic carbon (OC) content by dry combustion (Table 1). The water-holding capacity (WHC) was determined by pressure cooker as described by Klute (1986).
Atrazine Solution
Ring-U-labeled 14C-atrazine (radiopurity of >98%, specific activity = 7.77 x 108 Bq mmol-1) was purchased from Sigma (St. Louis, MO). Isotopic dilution with unlabeled atrazine was done in water solution with a final concentration of 26.5 mg L-1 and 2.95 106 Bq L-1.
14C-Atrazine Behavior
The behavior of 14C-atrazine was followed during laboratory incubations of 56 d at 28 ± 1°C in the dark. Triplicate incubations were done in hermetically closed glass jars. One milliliter of the 14C-atrazine solution was added to 10 g of dry soil. The soil water content was adjusted to 80% of the WHC (1.5 mL g-1) with Milli-Q water (Millipore, Billerica, MA) taking into account the atrazine solution. The 14C-CO2 evolved during the incubation was trapped in 2 mL of 2 M NaOH. The vials containing the NaOH were sampled and replaced after 3, 7, 15, 21, 28, 35, 42, 49, and 56 d. Atrazine mineralization was determined by measuring 14C-CO2 in the NaOH traps by scintillation counting with a Kontron (St. Quentin en Yvelines, France) Betamatic V liquid scintillation counter using Packard Ultima Gold XR as scintillation cocktail (PerkinElmer, Wellesley, MA).
After 7, 14, 28, and 56 d of incubation, 14C residues were extracted from the soil with 30 mL of methanol in glass centrifuge tubes. The tubes were agitated for 12 h on a rotative agitator at room temperature, then centrifuged 15 min at 5000 x g (Sorvall RC-5B centrifuge; Kendro Laboratory Products, Newtown, CT) and the supernatants were recovered. This extraction procedure was repeated three times. All supernatants were pooled and their 14C content was measured by scintillation counting as previously described.
After methanol extraction, soil pellets containing nonextractable 14C-atrazine residues were recovered and dried at 40°C. Dry samples were ground in a mechanical agate mortar. The radioactivity was measured on three subsamples (100–200 mg) by scintillation counting after combustion at 800°C under oxygen flow in a sampler oxidizer (Packard) followed by 14C-CO2 trapping in 8 mL of Carbosorb E (Packard), mixed with 12 mL of Permafluor E+ (Packard).
Methanol Extracts Analysis
The methanol extracts were concentrated by evaporation to near dryness under vacuum at 60°C using a Rotavapor (Büchi, Flawil, Switzerland), redissolved in 0.5 mL of mobile phase used for high performance liquid chromatography (HPLC) analysis, and filtered with a 0.45-µm nylon filter. All concentrated extracts were then analyzed by HPLC on a Nova-Pak C18 column (60 Å, 4 µm, 4.6 x 250 mm; Waters, Milford, MA) using a Waters appliance equipped with automatic injection and a 996 photodiode array detector coupled in-line with a radioactivity detector (Packard-Radioamatic Flo-One A-500). Packard UltimaFloAP was used as scintillating cocktail with a flow of 3 mL min-1. The mobile phase (1 mL min-1) was Solvent A (water, sodium dodecyl sulfate [SDS], 5 mM, pH adjusted to 2.8 with HCl) and Solvent B (water to methanol 1:9 v/v, SDS, 5 mM, pH adjusted to 2.8 with HCl). The gradient mobile phase is described by Loiseau et al. (2000). Dealkylated (deethyl-atrazine [DEA], deisopropyl-atrazine [DIA], and deethyl-deisopropyl-atrazine [DEDIA]) and hydroxylated (hydroxy-atrazine [OHAT], hydroxy-deethyl-atrazine [OHDEA], hydroxy-deisopropyl-atrazine [OHDIA], and hydroxy-deethyl-deisopropyl-atrazine [OHDEDIA]) metabolites were identified.
Soil Size Fractionation
At the end of the incubation period, the total residual radioactivity in the soil pellets after methanol extraction was measured as described above on three subsamples. Then, the residual triplicate soil pellets obtained after methanol extraction were pooled for particle size fractionation. Distilled water was added to the soil samples (soil to water 1:2) and 20 glass beads (0.5 cm in diameter) were added. The soil suspensions were agitated during 24 h on a rotative agitator, then the soil suspensions were passed through 200- and 50-µm sieves. The fractions 2000 to 200 and 200 to 50 µm were recovered and dried at 50°C. The suspension of particles smaller than 50 µm was centrifuged at 5000 x g and 4°C during 15 min. The supernatant containing part of the fraction of <2 µm was recovered and the soil pellet was resuspended in distilled water, sonicated (500 W) during 10 min, agitated during 12 h, then centrifuged at 175 x g and 4°C during 5 min to separate the 50- to 2-µm fraction. This procedure was repeated until clearness of the supernatant. The 50- to 2-µm pellets were dried at 50°C. All the supernatants were pooled and the fraction of <2 µm was recovered by overnight flocculation adding solid CaCl2 to reach 0.01 M final concentration, then centrifugation at 5000 x g and 4°C during 5 min and dried at 50°C. All dried samples were ground in a mechanical agate mortar and their radioactivity was measured in triplicate after combustion as previously described above.
Total Microbial Activity
To assess the total microbial activity (TMA), incubations of only 35 d were realized at 28 ± 1°C in the dark. Triplicate incubations were realized in hermetically closed glass jars. Milli-Q water was added to 10 g of dry soil, enough to set to 80% of the WHC. The C-CO2 evolved during the incubation was trapped in 2 mL of 2 M NaOH. The vials containing the NaOH were sampled and replaced after 3, 7, 15, 21, 28, and 35 d. The total C-CO2 produced by microbial activity and resulting from SOM mineralization was analyzed in the NaOH traps by colorimetry using a continuous flow analyzer (Skalar, Breda, the Netherlands).
Statistical Analysis
Statistical analysis consisted of determination of means and standard deviations and correlation analysis.
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RESULTS AND DISCUSSION
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14C-Atrazine Mineralization
The kinetics and rates of 14C ring-labeled atrazine mineralization are shown in Fig. 2
. Rapid atrazine mineralization was only observed in S1, a no-tilled soil cropped with a maize–soybean rotation, thus receiving atrazine in field conditions every other year. In this soil, atrazine mineralization reached 50% of the initially applied amount after 28 d of incubation. The mineralization rate (percentage of initial 14C-CO2 per day) increased up to Day 14, in relation to the development of the degrading microflora (Barriuso and Houot, 1996). Then the mineralization rate decreased and 62% of the initial atrazine was mineralized at the end of the incubations. Accelerated mineralization of a pesticide occurred after repeated use of the same molecule due to the adaptation of the soil microflora (Leistra and Green, 1990). This has also been documented previously for atrazine in several soils (Stolpe and Shea, 1995; Topp et al., 1995; Barriuso and Houot, 1996; Vanderheyden et al., 1997; Jenks et al., 1998; Wenk et al., 1998; Abdelhafid et al., 2000a; Houot et al., 2000).
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Fig. 2. (a) Kinetics of 14C-atrazine mineralization and (b) evolution of mineralization rates during incubation of 14C-atrazine in the four soils.
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In the other soils without field atrazine application, the atrazine mineralization was similar and much lower than in S1. At the end of the incubation period, the percentages of 14C-CO2 released were 11.3, 12.0, and 10.9% in S2, S3, and S4, respectively. This would indicate that the soil tillage management did not influence atrazine mineralization, which remained similar to a natural uncultivated soil. Our results confirmed that the accelerated atrazine mineralization primarily depended on the atrazine history of the soils.
Atrazine mineralization was not related to TMA (Houot et al., 1998). Similar rates of atrazine mineralization were observed in S4 although it presented a larger TMA as revealed by the kinetics of organic matter mineralization (Fig. 3)
. The differences in TMA were directly related to the differences in total SOM, larger in S4 than in S2 and S3. Although under no tillage for four years, S2 did not present a larger proportion of SOM than S3. No-tillage usually provokes an increase in SOM in the top centimeters of a soil. The sampling of soil at 20 cm may have diluted the surface accumulation of SOM.
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Fig. 3. Kinetics of total organic carbon (OC) mineralization during laboratory incubations of the four soils as an indicator of total microbial activity (TMA). The standard deviations (error bars) are shown when larger than the symbol size.
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Evolution of 14C Distribution between Mineralized, Extractable, and Nonextractable Residues during Incubation
The proportions of extractable 14C-residues decreased during the incubations in the four soils (Table 2). In S1, this decrease was more pronounced supporting the idea that the extractable fraction was the most available for microbial degradation (Johnson et al., 1999). The evolution of the extractable residues in the soils without field atrazine application under no-tillage (S2) and conventional tillage (S3) was similar, while the smallest proportion of extractable 14C residues at the end of the incubation period was found in the brushwood soil (S4).
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Table 2. Evolution of 14C-atrazine distribution into mineralized, extractable, and bound-residue fractions during incubation in the four soils.
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Rapid formation of nonextractable, so-called bound residues was observed in all soils (Table 2). After 7 d of incubation, more than 38% of the initial radioactivity was unextractable. In S1, the percentage of 14C bound residues remained rather constant throughout all the incubation period. Conversely, in the other soils (S2, S3, and S4), with no previous field atrazine application, the bound residue proportion increased. The largest proportion of bound residues was observed in the natural brushwood soil (S4), reaching 79.9% at Day 56. This could probably be related to its higher OC content (5.1%) and lower pH (5.4). Seybold et al. (1994) determined that soils developed under forest vegetation presented high retention indexes (Koc). They associated this behavior to the composition of the organic fraction of the forest soils. On the other hand, atrazine hydrolysis to hydroxy-atrazine (OHAT) in soils is enhanced by sorption to soil colloids (Jordan et al., 1970) or conditions of acidity (Martín-Neto et al., 2001). Hydroxy-atrazine presents higher indices of retention and higher desorption hysteresis than atrazine and the other dealkylated metabolites (Moreau and Mouvet, 1997). It is possible that S4 characteristics (higher OC content and lower pH) favor OHAT formation and that this metabolite is the main component of bound residues. Regarding bound residues composition, Loiseau (2001) determined that in soils with pH 
6 more than the 60% of the bound residues are hydroxy-metabolites. Similar results were obtained previously by Lerch et al. (1997)(1999), who replaced methanol by a mixed-mode extractant, recovering 60% more extractable residues, of which OHAT was the main component (74%). On the other hand, the high microbial activity of S4 could also partly explain the formation of bound residues by the microbial biomass (Bollag and Liu, 1990; Abdelhafid et al., 2000b). The formation of nonextractable residues was similar in S2 and S3, a fact that could be explained in part by their similar OC content.
Extractable Residues Composition
Atrazine was the major constituent in all the extractable fractions, at all incubation periods and in all management systems (Table 2). Atrazine half-life time was calculated using the first-order equation Ct = C0 exp(-kt), where Ct is the concentration of atrazine at time t, C0 is the initial atrazine concentration, k is the dissipation rate, and t is the time of measurement. The t1/2 values obtained were 16, 41, 40, and 31 d for S1, S2, S3, and S4, respectively. The lowest t1/2 values calculated in S1 support the importance of soil atrazine history in the development of a degrading microflora. On the other hand, no effect of the tillage management on the kinetics of atrazine dissipation was observed in S2 and S3, as previously reported by Shelton et al. (1998). The brushwood soil (S4) showed a lower atrazine t1/2 than the cultivated soils without field atrazine application (S2 and S3). In this soil, both atrazine mineralization and formation of bound residues contributed to atrazine dissipation.
After 28 d of incubation, the metabolites represented 71% of the total extractable radioactivity in S1, related to the intense microbial transformation in this soil. In the other soils, metabolites represented only 53, 34, and 23% of the extractable radioactivity in S2, S3, and S4, respectively.
The proportions of the different metabolites in the extractable fractions were similar in the four soils. The metabolites deethyl-deisopropyl-atrazine (DEDIA), deethyl-atrazine (DEA), and OHAT were the most abundant. Less deisopropyl-atrazine (DIA) was recovered than DEA. The proportions of DEA decreased during incubation while that of OHAT increased. The proportions of atrazine hydroxy-dealkylated metabolites varied between 0.1 and 1.3% of the initial radioactivity in all soils. Other more polar atrazine metabolites were detected in trace proportions. After 56 d of incubation, most metabolites were undetectable in the extracts.
Distribution of 14C-Bound Residues in Soil Size Fractions
After extraction of 14C residues, soil size fractionation was done directly without OC elimination. The mass balance of the fractions was good (>97%) but the distribution among the different soil size fractions differed from the results of the classical granulometric analysis done after OC destruction (Table 3). In S4 with the highest OC content, the 50- to 2-µm fraction was overestimated and the 2000- to 50- and <2-µm fractions underestimated as compared with granulometrical results (Fig. 4a) . The cropped soil with the highest OC content (S1) presented the same tendency. On the contrary, in S2 and S3 the <2-µm fraction was overestimated and the 50- to 2-µm fraction underestimated.
The coarsest soil size fractions (2000–200 and 200–50 µm) containing the nonhumified SOM (Christensen, 1992) presented the largest OC content with the exception of S2 (Fig. 4b). However, because of the soil size distribution, only approximately 20% of SOM was found in the coarsest fraction for the cultivated soils (Table 3). In the natural soil (S4), the nonhumified fraction represented 47% of SOM.
The largest concentration of 14C-atrazine bound residues expressed as µg of 14C-atrazine equivalent per g of fraction was found in the fraction 2000 to 200 µm in S1, S3, and S4 (Fig. 5)
as usually found for atrazine (Barriuso and Koskinen, 1996). In S2, the concentration in bound residues of each soil size fraction was similar. In all soils, the smallest concentrations of bound residues were found in the 50- to 2-µm fraction.
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Fig. 5. Amount of atrazine-bound residues, in the different soil size fractions, expressed as 14C-atrazine equivalent per g of fraction.
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The concentration of 14C-atrazine bound residues increased with the OC content of the fractions, with strong correlation (r = 0.92; p < 0.000).
To assess the preferential accumulation of bound residues in each soil size fraction, the ratio between the bound residue content in each fraction and the bound residue content in whole soil was calculated (Fig. 6)
. Values larger than 1 indicated the accumulation of bound residues in the fraction. The largest enrichments were observed in the coarsest fractions containing the nonhumified SOM. In all soils, only the 50- to 2-µm fraction presented a deficit in bound residue formation compared with the whole soils. No-tillage soil management, which favored low humified organic matter accumulation, could allow a higher bound residue formation. However, in our results soil management did not differentiate nonhumified organic matter with different capacities to form bound residues.
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Fig. 6. Relative enrichment of atrazine-bound residues in relation to fraction size. Relative enrichment is defined as the ratio between the content in fraction and the content in the whole soil.
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CONCLUSIONS
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Repeated use of atrazine in field conditions was the most influential management factor in atrazine evolution in soil. Atrazine application is related to the introduction of maize in the crop rotation. Its application every other year in the maize–soybean rotation was enough to develop an adapted microflora able to mineralize triazine rings. Atrazine stabilization as bound residues in the soil was a fast process, which depended on SOM content. The nonhumified organic matter, localized in the >50-µm fractions, presented the largest capacity to form bound residues. No differences were observed in atrazine behavior in no-tilled or tilled soils, probably because of the sampling in the upper 20 cm. Due to strong stratification of organic matter in soils under no-tillage systems, it should be necessary to do the soil sampling and to study atrazine behavior following the stratification pattern of the SOM.
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ACKNOWLEDGMENTS
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This work was granted by the Programa de Cooperación Franco–Argentino ECOS SUD-SETCYP, A00U01.
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ABSTRACT
INTRODUCTION
