Letter Cite This: Environ. Sci. Technol. Lett. XXXX, XXX, XXX−XXX
pubs.acs.org/journal/estlcu
Occurrence of Dichloroacetamide Herbicide Safeners and Co-Applied Herbicides in Midwestern U.S. Streams Emily E. Woodward,*,† Michelle L. Hladik,† and Dana W. Kolpin‡ †
U.S. Geological Survey, 6000 J Street, Placer Hall, Sacramento, California 95819, United States U.S. Geological Survey, 400 South Clinton Street, Iowa City, Iowa 52240, United States
‡
S Supporting Information *
ABSTRACT: Dichloroacetamide safeners (e.g., AD-67, benoxacor, dichlormid, and furilazole) are co-applied with chloroacetanilide herbicides to protect crops from herbicide toxicity. While such safeners have been used since the early 1970s, there are minimal data about safener usage, occurrence in streams, or potential ecological effects. This study focused on one of these research gaps, occurrence in streams. Seven Midwestern U.S. streams (five in Iowa and two in Illinois), with extensive row-crop agriculture, were sampled at varying frequencies from spring 2016 through summer 2017. All four safeners were detected at least once; furilazole was the most frequently detected (31%), followed by benoxacor (29%), dichlormid (15%), and AD-67 (2%). The maximum concentrations ranged from 42 to 190 ng/L. Stream detections and concentrations of safeners appear to be driven by a combination of timing of application (spring following herbicide application) and precipitation events. Detected concentrations were below known toxicity levels for aquatic organisms.
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INTRODUCTION Herbicide safeners (antidotes) are co-applied with herbicides to protect crops from herbicide toxicity.1,2 A few working hypotheses exist around the safener mode of action within the crop; the predominant hypothesis is that the safener activates plant defense genes within the crop.3 The plant responds by increasing production of the enzymes responsible for herbicide detoxification;4,5 the herbicide is metabolized, and the crop is protected from herbicide injury. The first commercial use of an herbicide safener was in 1971 (1,8naphthalic anhydride).2,6 Since then, ∼20 safeners have been developed.7 This research focuses on four dichloroacetamide safener compounds that are used in corn (Zea mays L.) production: AD-67, benoxacor, dichlormid, and furilazole.8−10 By design, these four safeners should be applied as part of a formulation with either a chloroacetanilide or thiocarbamate herbicide and a number of additional ingredients.4,5,8,11 They are typically paired with the chloroacetanilide herbicides acetochlor and/or metolachlor (Table 1), and at least for benoxacor and dichlormid, they represent 14% (by mass) of the formulation relative to the herbicide.10 Dichloroacetamide safeners and herbicides are co-applied via spraying onto the soil at the pre-plant stage or at the preemergence stage of the planting season.7 On the basis of the chemical data available for these four safeners, there is potential for transport within the soil or transport off site (Table 1). These safeners degrade via microbial degradation in the soil, and the aerobic half-lives (DT50) range from 7 to 50 days.10,12 The reported log Kow values for these safeners range from 1.84 to 3.19, which are similar to those of the co-applied hebicides © XXXX American Chemical Society
(the log Kow values for acetochlor and metolachlor are 4.14 and 3.05, respectively).10,12 The limited sorption data available suggest low sorption: the Kd for dichlormid ranges from 0.25 to 0.65 mL/g and the Kd for furilazole from 0.79 to 3.5 mL/g.10 With similar physicochemical properties, the safeners are likely to be as mobile as the herbicides with which they are coapplied. While herbicide safeners are considered “inert” compounds, from a regulatory perspective they are, in fact, biologically active.10 They exhibit a low to moderate reported toxicity to aquatic organisms (LC50 values for freshwater fish range from 1.4 to 4.6 mg/L),12 and studies have reported an increase in freshwater fish (Pimephales promelas) sensitivity after exposure for 32 days.13 The compounds furilazole and AD-67 are classified by the U.S. Environmental Protection Agency as “likely to be carcinogenic to humans” after oral exposure.14,15 In addition, such safeners add to the overall complexity of chemical mixtures to which aquatic organisms and microorganisms are exposed. These chemical mixtures have the potential to be more toxic to nontarget organisms than the individual chemicals that comprise such mixtures.16,17 Furthermore, one study found that in iron-reducing environments dichloracetamide sanfeners can form herbicide active derivatives, creating another potential toxicity pathway.18 Overall, the ecological toxicity data for safeners constitute one of the many Received: Revised: Accepted: Published: A
November November November November
9, 2017 29, 2017 30, 2017 30, 2017 DOI: 10.1021/acs.estlett.7b00505 Environ. Sci. Technol. Lett. XXXX, XXX, XXX−XXX
Letter
Environmental Science & Technology Letters Table 1. Select Physical Properties for the Dichloroacetamide Safeners
a
Structures made in ChemDraw. bUnless otherwise cited, data from Pesticide Property DataBase (University of Hertfordshire, Hertfordshire, U.K.).12 cFrom ref 10.
Figure 1. Distribution of the seven sampling sites and their associated watersheds in Iowa and Illinois.
B
DOI: 10.1021/acs.estlett.7b00505 Environ. Sci. Technol. Lett. XXXX, XXX, XXX−XXX
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Environmental Science & Technology Letters
Figure 2. Safener concentration ranges for the seven sampling sites in Iowa and Illinois. Sites are arranged from top left to bottom right by drainage area. Detection frequencies for each compound and each site can be found in Table S1. ND, not detected.
from the Iowa River were collected on a biweekly to monthly basis. Samples were shipped on ice to the laboratory. Laboratory Extraction and Analysis. Upon arrival at the laboratory, all 1 L samples were filtered through prebaked, 0.7 μm glass fiber filters (GF/F, Whatman, Florham Park, NJ). Samples were spiked with the surrogate compound d14triflurlain (Cambridge Isotope, Andover, MA) at a concentration of 200 ng/L. Samples were processed through an Oasis MAX solid-phase extraction (SPE) cartridge (6 cm3, 500 mg; Waters Corp., Milford, MA) following a previously described Oasis HLB method.23 The ethyl acetate eluent (12 mL) from the SPE was reduced to 200 μL under nitrogen and spiked with 20 μL of internal standard (d10-acenaphthene; Cambridge Isotope). Samples were analyzed on an Agilent (Santa Clara, CA) 7890 A gas chromatogram (GC) coupled to a model 5975 C inert XL EI/CI mass spectrometer run in EI mode. The limit of detection (LOD) for each safener and herbicide was 2 ng/L, and the method reporting limit (MRL) was 6 ng/L. More details about extraction recoveries and the gas chromatography−mass spectrometry conditions are provided in the Supporting Information.
research gaps in the literature. Additional research gaps include data on safener usage, metabolite formation, metabolite fate, and environmental occurrence. The objective of this study was to focus on the environmental occurrence data gap by providing first-ever baseline data for dichloroacetamide safener concentrations in streams. A total of 192 water samples from seven sites of varying basin size [12−32400 km2 (Table S1)] across Iowa and Illinois were collected and analyzed for AD-67, benoxacor, dichlormid, and furilazole and two co-applied herbicides (acetochlor and metolachlor). Data from this study will help researchers (1) define potential exposure of herbicide safeners in an agricultural setting, (2) document the temporal nature of such safener exposures, (3) better characterize the water quality effects from herbicide applications, and (4) help direct future toxicity and ecological studies focused on herbicide and herbicide safeners.
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EXPERIMENTAL METHODS Site Selection and Sampling. A total of 5.6 million ha in Iowa and 4.7 million ha in Illinois are in corn (Zea mays L.) production, the top two states in corn production in the United States.19,20 In 2016, 4 million lb of acetochlor (26% of corn in state) and 5 million lb of metolachlor (38% of corn in state) were applied to corn in Illinois, and 9 million lb of acetochlor (46% of corn in state) and 5 million lb of metolachlor (23% of corn in state) were applied to corn in Iowa.21 As the dichloroacetamide safeners included in this study are coapplied with these two herbicides, Iowa and Illinois streams were ideal for determining the potential for off-field transport of the four target dichloroacetamide safeners. Stream sites that drained predominantly agricultural basins ranging in size from 12 to 32400 km2 were selected (Figure 1). Sites chosen were representative of small streams and large rivers in Iowa and Illinois. Grab or depth−width integrated composite 1 L water samples were collected in amber glass bottles.22 Iowa samples were collected from March 2016 to June 2017 and captured consecutive growing seasons (Figure S1). Illinois samples were collected from September 2016 to June 2017 and captured one growing season. With one exception (Iowa River), all sites were sampled using a hydrologic-based approach to collect samples near peak flow during storm events (capturing overland flow) and periodic samples during base flow conditions. Samples
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RESULTS AND DISCUSSION Overall, at least one of the four safeners was detected (greater than or equal to the LOD) in 43% of samples (82 samples had detects of 192 collected). Within the 82 samples that had safener detections, 52% had at least two safeners present, 21% had at least three present, and no samples had all four safeners present (Table S2). AD-67 was detected at one of the seven sites (Figure 2), with an overall detection frequency of 2% (3 of 192 samples) and concentrations ranging from 45 to 79 ng/L (Table S2). Dichlormid was detected at five of the seven sites (Figure 2), with an overall detection frequency of 15% (28 of 192 samples) and concentrations ranging from 5 to 42 ng/L (Table S2). Benoxacor was detected at seven of the seven sites (Figure 2), with an overall detection frequency of 29% (55 of 192 samples) and concentrations ranging from 4 to 190 ng/L (Table S2). Furilazole was detected at seven of the seven sites (Figure 2), with an overall detection frequency of 31% (59 of 192 samples) and concentrations ranging from 4 to 150 ng/L (Table S2). Detection frequencies vary by site (Table S1), and in certain cases, the site specific detection frequency is greater than the overall detection frequency. C
DOI: 10.1021/acs.estlett.7b00505 Environ. Sci. Technol. Lett. XXXX, XXX, XXX−XXX
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Environmental Science & Technology Letters
Figure 3. Concentrations of benoxacor, dichlormid, and furilazole, the herbicides acetochlor and metolachlor, and stream discharge for the English River (05455500), from March 2016 to June 2017. AD-67 was not detected at this site. The shaded area is the typical corn planting season in Iowa.
based sampling sites, higher safener concentrations were generally seen during storm events at or near peak flow conditions (Table S2, Figure 3, and Figures S2−S4, S6, and S7). This indicates that overland flow is a possible source of safeners in streams. With the exception of AD-67, the safeners were detected in both Iowa and Illinois sampling sites (Table S1). With the exception of the Iowa River, which was not sampled using a hydrologic-based sampling approach, safener detection frequencies and concentrations were generally higher at the Iowa sites than at the Illinois sites (Table S1). This could be the result of (1) the sampling frequency and/or (2) the length of the sampling period. The Iowa sites were sampled more frequently than the Illinois sites, especially during the spring field season. In addition, the Iowa sites were sampled over the entire year (March 2016 to June 2017) and captured two spring field seasons (Figure 3 and Figures S2−S4). The Illinois sites were sampled for only part of the year (September 2016 to June 2017) and captured only one spring field season (Figures S6 and S7). In addition to the four herbicide safeners, the co-applied herbicides acetochlor and metolachlor were measured in the 192 samples that were collected. These herbicides were chosen as a reference because (1) they are the two herbicides that are co-formulated with the dichloroacetamide safeners in this study and (2) they represent another class of organic pollutants that have a history of heavy usage on corn crops, off-field transport, and high detection frequencies and concentrations in streams.26 Both herbicides were ubiquitiously detected in the samples collected. Metolachlor was detected in 100% of the samples, while acetochlor was detected in 73% of the samples; detected concentrations ranged from 10 to 15000 ng/L (Table S2). Acetochlor and metolachlor were detected more frequently and
Results from this study document a clear relationship between safener detection and timing of corn planting (Table S2). Safeners are co-applied with herbicides at either the preplant (prior to the corn crop being planted) or pre-emergence (prior to the corn and/or weed plant emerging from the ground) stage of the planting season.7 According to the U.S. Department of Agriculture,24 the corn planting windows for Iowa were mid-April to late May in 2016 and late April to late May in 2017 (Figure 3 and Figures S2−S5). The corn planting windows for Illinois were early April to early June 2017 (Figures S6 and S7).25 Exact corn planting dates and herbicide application times vary within the spring months by farm and region and depend heavily on the farm soil conditions and regional weather patterns. For the most part, the first detection of dichloroacetamide safeners in streams correlates to the preplant and/or pre-emergent safener application window, and detections continued beyond the safener application period (through June) (Figure 3 and Figures S2−S7). This suggests that safeners can be transported off site for several weeks after applications have ceased, with sporadic pulses in more distal periods following application. Overall, only 13 of the 145 detections occurred outside of the spring months of March− June (Table S2, Figure 3, and Figures S2−S6); the largest number of detections occurred in the month of May when the largest amounts of corn are planted (Table S2). Of the 17 samples that had three or more detections (benoxacor, dichlormid, and furilazole), 14 were collected in the month of May. Samples with multiple detections and the highest concentrations also tended to correspond with a storm event (Table S2). Results from this study document a temporal relationship among safener stream detections, safener concentrations, and storm events (Figure 3 and Figures S2−S7). At the hydrologicD
DOI: 10.1021/acs.estlett.7b00505 Environ. Sci. Technol. Lett. XXXX, XXX, XXX−XXX
Letter
Environmental Science & Technology Letters had concentrations higher than those of the herbicide safeners, which likely relates to the mass applied.10 However, for samples with safener detections, a statistical correlation (Pearson) existed between each safener and the specific herbicide with which each is co-applied with: furilazole and acetochlor (r = 0.85; p < 0.001), dichlormid and acetochlor (r = 0.53; p = 0.004), and benoxacor and metolachlor (r = 0.43; p = 0.001). Safener concentrations increased with increasing concentrations of the associated herbicide. The safeners exhibited a spring flush during spring and early summer rainfall events, a trend that is well-documented for herbicides.26,27 Data about the potential effects of this pulse of safeners into streams on aquatic organisms are limited. The available data are focused on benoxacor and furilazole.10 The benoxacor and furilazole concentrations measured in this study (≤190 ng/L) were orders of magnitude below the reported LC50 toxicity levels for freshwater algae (0.63 mg/L for benoxacor) and freshwater fish (1.4 mg/L for benoxacor and 4.6 mg/L for furilazole).10,13 These are acute toxicity levels. Literature data defining chronic toxicity levels do not exist. One study documented an increase in freshwater fish sensitivity after a 32 day exposure to benoxacor, at a no observed effect concentration of 0.31 mg/L.13 Concentrations measured in this study were also well below this lower effect level. From these limited studies, there appears to be minimal risk of safeners to algae and fish. However, there is still uncertainty about how these safeners affect aquatic organisms in a mixture with other safeners and in a mixture with other contaminants.16,28 One study documented that the total herbicide and benoxacor formulation, containing a number of compounds at low concentrations, was more toxic to aquatic organisms than individual compounds were within the formulation.16 In general, more ecotoxicity research on formulations and individual safeners is needed, and data from this study can help guide future effects research. This study was the first to document off-field transport of dichloroacetamide safeners to streams. Detected safener concentrations were several orders of magnitude below known acute toxicity levels for aquatic organisms, but the long-term and mixture effects on nontarget aquatic and microbial organisms are still unknown. Detections and stream concentrations appear to be driven by the timing of application and precipitation. Safeners and herbicides appear to follow similar spring flushing patterns. When herbicides are detected in streams, it is likely that safeners are present as well, albeit at much lower concentrations. Results from this study highlight the fact that while safeners are transporting off-field, the detected levels (nanograms per liter) pose a minimal risk to aquatic organisms.
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sites, West Branch Wapsinonoc Creek (Figure S2), Old Mans Creek (Figure S3), Clear Creek (Figure S4), Iowa River (Figure S5), Spoon River (Figure S6), and Vermilion River (Figure S7) (PDF)
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. ORCID
Emily E. Woodward: 0000-0001-9196-1349 Michelle L. Hladik: 0000-0002-0891-2712 Dana W. Kolpin: 0000-0002-3529-6505 Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This research was funded by the U.S. Geological Survey (USGS) Toxic Substances Hydrology Program. We thank our USGS colleagues Shannon Meppelink and Paul Terrio for assisting with sample collection for this study and Matt De Parsia for help with sample processing. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government. Data presented in this manuscript can also be accessed here: Woodward, E. E.; Hladik, M. L.; Kolpin, D. W. Herbicide Safener and Co-Applied Herbicide Concentrations for Seven Streams across Iowa and Illinois (March 2016 to June 2017). U.S. Geological Survey data release, 2017, DOI: 10.5066/ F7CZ363N.
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REFERENCES
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.estlett.7b00505. Experimental methods, including quality assurance, site specific drainage area, and detection frequencies for each compound (Table S1), stream discharge and concentrations of each compound for each sample (Table S2), mass spectrometry ions (Table S3), temporal photos documenting stream and crop conditions during the sampling period for West Branch Wapsinonoc Creek (Figure S1), and hydrographs for the remaining sampling E
DOI: 10.1021/acs.estlett.7b00505 Environ. Sci. Technol. Lett. XXXX, XXX, XXX−XXX
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Environmental Science & Technology Letters (12) PPDB: Pesticide Properties Database (University of Hertfordshire). https://sitem.herts.ac.uk/aeru/ppdb/en/ (accessed August 11, 2017). (13) European Chemicals Agency. https://echa.europa.eu/ information-on-chemicals (accessed August 11, 2017). (14) Cancer Assessment Document for MON 13900. Evaluation of the carcinogenic potential of MON 13900. Technical Report; U.S. Environmental Protection Agency: Washington, DC, 1999 (https:// www3.epa.gov/pesticides/chem_search/cleared_reviews/csr_PC911596_15-Oct-99_001.pdf) (accessed August 11, 2017). (15) Proposition 65 MON 4660: Chemicals considered or listed under proposition 65. Technical Report; California Environmental Protection Agency: Sacramento, CA, 2011 (https://oehha.ca.gov/ proposition-65/proposition-65-list) (accessed August 11, 2017). (16) Joly, P.; Bonnemoy, F.; Charvy, J.; Bohatier, J.; Mallet, C. Toxicity assessment of the maize herbicides S-metolachlor, benoxacor, mesotrione and nicosulfuron, and their corresponding commercial formulations, alone and in mixtures, using the Microtox® test. Chemosphere 2013, 93, 2444−2450. (17) Escher, B. I.; Hermens, J. L. M. Modes of action in ecotoxicology: their role in body burdens, species sensitivity, QSARs, and mixture effects. Environ. Sci. Technol. 2002, 36, 4201− 4217. (18) Sivey, J. D.; Roberts, A. L. Abiotic reduction reactions of dichloroacetamide safeners: transformations of “inert” agrochemical constituents. Environ. Sci. Technol. 2012, 46, 2187−2195. (19) Iowa Agriculture Overview 2016. Technical Report; U.S. Department of Agriculture: Washington, DC, 2017 (https://www. nass.usda.gov/Statistics_by_State/Iowa/index.php) (accessed August 2, 2017). (20) Illinois Agriculture Overview 2016. Technical Report; U.S. Department of Agriculture: Washington, DC, 2017 (https://www. nass.usda.gov/Statistics_by_State/Illinois/index.php) (accessed August 2, 2017). (21) Agricultural Chemical Use Survey: Corn Data Tables 2016. Technical Report; U.S. Department of Agriculture: Washington, DC, 2017 (https://www.nass.usda.gov/Surveys/Guide_to_NASS_ Surveys/Chemical_Use/) (accessed August 2, 2017). (22) U.S. Geological Survey. Collection of water samples (version 2.0): U.S. Geological Survey Techniques of Water-Resources Investigations; Book 9, Chapter A4, 2006 (https://water.usgs.gov/owq/FieldManual/ chapter4/html/Ch4_contents.html) (accessed August 11, 2017). (23) Hladik, M. L.; Smalling, K. L.; Kuivila, K. M. A multi-residue method for the analysis of pesticides and pesticide degradates in water using HLB solid-phase extraction and gas chromatography-ion trap mass spectrometry. Bull. Environ. Contam. Toxicol. 2008, 80, 139−144. (24) Iowa Crop Progress & Conditions Report. Technical Report; U.S. Department of Agriculture: Washington, DC, 2017 (https:// www.nass.usda.gov/Statistics_by_State/Iowa/Publications/) (accessed August 14, 2017). (25) Illinois Crop Progress & Conditions Report. Technical Report; U.S. Department of Agriculture: Washington, DC, 2017 (https:// www.nass.usda.gov/Statistics_by_State/Illinois/index.php) (accessed August 14, 2017). (26) Battaglin, W. A.; Thurman, E. M.; Kalkhoff, S. J.; Porter, S. D. Herbicides and transformation products in surface waters of the Midwestern United States. J. Am. Water Resour. Assoc. 2003, 39, 743− 756. (27) Thurman, E. M.; Goolsby, D. A.; Meyer, M. T.; Kolpin, D. W. Herbicides in surface waters of the Midwestern United States: the effect of spring flush. Environ. Sci. Technol. 1991, 25, 1794−1796. (28) Bolyard, K.; Gresens, S. E.; Ricko, A. N.; Sivey, J. D.; Salice, C. J. Assessing the toxicity of the “inert” safener benoxacor toward Chironomus riparius: effects of agrochemical mixtures. Environ. Toxicol. Chem. 2017, 36, 2660−2670.
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