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Direct Photolysis Rates and Transformation Pathways of the Lampricides TFM and Niclosamide in Simulated Sunlight Megan B. McConville,† Terrance D. Hubert,‡ and Christina K. Remucal*,†,§ †

Environmental Chemistry and Technology Program, University of Wisconsin − Madison, Madison, Wisconsin 53706, United States Upper Midwest Environmental Sciences Center, United States Geological Survey, La Crosse, Wisconsin 54603, United States § Department of Civil and Environmental Engineering, University of Wisconsin − Madison, Madison, Wisconsin 53706, United States ‡

S Supporting Information *

ABSTRACT: The lampricides 3-trifluoromethyl-4-nitrophenol (TFM) and 2′,5-dichloro-4′-nitrosalicylanilide (niclosamide) are directly added to many tributaries of the Great Lakes that harbor the invasive parasitic sea lamprey. Despite their long history of use, the fate of lampricides is not well understood. This study evaluates the rate and pathway of direct photodegradation of both lampricides under simulated sunlight. The estimated half-lives of TFM range from 16.6 ± 0.2 h (pH 9) to 32.9 ± 1.0 h (pH 6), while the half-lives of niclosamide range from 8.88 ± 0.52 days (pH 6) to 382 ± 83 days (pH 9) assuming continuous irradiation over a water depth of 55 cm. Both compounds degrade to form a series of aromatic intermediates, simple organic acids, ring cleavage products, and inorganic ions. Experimental data were used to construct a kinetic model which demonstrates that the aromatic products of TFM undergo rapid photolysis and emphasizes that niclosamide degradation is the rate-limiting step to dehalogenation and mineralization of the lampricide. This study demonstrates that TFM photodegradation is likely to occur on the time scale of lampricide applications (2−5 days), while niclosamide, the less selective lampricide, will undergo minimal direct photodegradation during its passage to the Great Lakes.

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compared to native aquatic species.1,3,6 Niclosamide, in contrast, was developed as a molluscide and is not selective to the sea lamprey.2,5 Both compounds have been used since the 1960s to target the invasive parasite.11 Approximately 50,000 kg of TFM are added to Great Lakes tributaries every year at concentrations ranging from 4.8 to 67.6 μM active ingredient.11−13 Niclosamide is generally added as 1% by weight to TFM in larger tributaries to enhance the effectiveness of TFM and reduce the amount of TFM required, thereby reducing the cost of treatment.12,14−17 The lampricides are added directly to tributaries for up to 12 h to ensure that the minimum lethal concentration is maintained in each stream section for at least 9 h, resulting in acute toxicity to the sea lamprey.14 TFM and niclosamide concentrations are monitored during lampricide applications by UV−visible spectroscopy and high performance liquid chromatography (HPLC), respectively; additional lampricide is added to ensure that the target concentration is maintained throughout the treatment. Lampricides are generally applied to sea lamprey larvae-infested tributaries every 2−5 years, with the goal of targeting multiple generations of sea lamprey.13,18 Although the

INTRODUCTION The sea lamprey, Petromyzon marinus, is an invasive species in the Great Lakes that preys on large fish, including lake trout, whitefish, and cisco, and was partially responsible for the decline of the Great Lakes fisheries in the 1940s and 1950s.1−4 The fish entered the Great Lakes from the Atlantic Ocean through manmade shipping canals and has been documented in all of the Great Lakes since the late 1930s.1−6 The sea lamprey begins its life as a nonparasitic filter-feeding larva in freshwater streams and has been identified in over 400 tributaries of the Great Lakes.1 After 18 months to eight years,1,7 the sea lamprey reaches maturity, undergoes metamorphosis to become parasitic, and migrates downstream to the Great Lakes in search of hosts. Control strategies, such as the use of traps and barriers to prevent upstream migration1 and the use of pheromones to enhance trapping,8−10 are used to combat the invasive species. These approaches focus on limiting adult sea lamprey spawning in tributaries. Although these management practices play a role in sea lamprey control, the most widely used strategy is the application of two chemical lampricides, 3-trifluoromethyl-4nitrophenol (TFM) and 2′,5-dichloro-4′-nitrosalicylanilide (niclosamide; Scheme 1), which are designed to kill larval sea lamprey in freshwater tributaries where they are applied. TFM was selected from a group of over 6000 chemicals based on tests that demonstrated its selective toxicity toward sea lamprey © XXXX American Chemical Society

Received: May 24, 2016 Revised: August 10, 2016 Accepted: August 10, 2016

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DOI: 10.1021/acs.est.6b02607 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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Environmental Science & Technology Scheme 1. Proposed Photodegradation Pathway of TFM and Niclosamidea

Products denoted with ∗ were detected by Graebing et al.2 Intermediates identified with † were proposed by Carey and Fox.22 Products denoted with ∗∗ were identified by Ellis and Mabury.13 Underlined products were quantified in this study. Percentages represent the fraction of each compound that proceeds via the indicated pathways as determined using kinetic modeling.

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MATERIALS AND METHODS Materials. All chemicals were used as received from the manufacturers (Supporting Information; Section S1). Ultrapure water was supplied by a Milli-Q water purification system maintained at 18.2 MΩ cm. Solution Preparation. Samples for each photochemical experiment were prepared in 2−5 mM acetate (pH 4−5), phosphate (pH 6−7), or borate (pH 8−9) buffer solutions. Buffer solutions were fortified with either TFM or niclosamide to a nominal concentration of 1−10 μM. Additionally, the direct photodegradation rates of the proposed intermediate lampricide photoproducts were separately quantified at pH 8 starting with an initial 10 μM concentration. These products include 2-chloro4-nitroaniline (2Cl4NA), 2-chloro-4-nitrophenol (2Cl4NP), 4nitrocatechol (4NCat), 4-hydroxycatechol (4OHCat), 5-chlorosalicylic acid (5ClSA), gentisic acid (GA), and maleic acid (MA). Trifluoroacetic acid (TFA) was also evaluated as a product of TFM photolysis. Photochemical Experiments. Most photochemical experiments were performed in a Rayonet merry-go-round photoreactor equipped with 16 fixed-wavelength bulbs with a maximum irradiance at 365 nm (width at half-maximum = ±9 nm),34 which is within the spectrum of natural sunlight (Sections S2 and S3). Experiments were conducted in triplicate in quartz test tubes that were sealed with cork stoppers. A portion of each solution was kept in the dark as a control. Throughout the irradiation, aliquots were collected from each test tube for subsequent analysis. The temperature in the photoreactor could not be controlled and was 31.3 ± 1.8 °C during irradiations (Figure S4). Most dark control samples were held at ambient temperatures (25 °C ± 1 °C), with a subset of control experiments conducted under the elevated temperatures in the photoreactor. Degradation of the parent compounds were not observed in any of the dark controls (data not shown). A limited number of niclosamide experiments were conducted with a 450 W xenon lamp, which has a spectrum similar to that of sunlight when the appropriate cutoff filters are used (Section S2). An actinometer solution consisting of 10 μM para-nitroanisole in 1 mM pyridine was irradiated side-by-side with the target compounds to quantify the intensity of both light sources.35 Initial experiments were conducted from pH 4−9 to assess the impact of pH on the photodegradation rates of TFM and

use of chemical lampricides as a management strategy has been highly effective at controlling sea lamprey populations, there may be potential negative impacts to nontarget species.14,19,20 For example, TFM can be toxic to sturgeon,19,20 while niclosamide negatively impacts channel catfish, yellow perch, and molluscs.14 For this reason, there is a need to better understand the fate and persistence of these compounds and their transformation products in the aquatic environment. The environmental fate of TFM and niclosamide in natural waters is not fully understood. Neither compound is subject to hydrolysis or volatilization.16,19,18,21,22 While both compounds can bind to sediments in a reversible and pH-dependent manner, sorption is generally more important for niclosamide than TFM.14,16,19,23−27 Although several studies indicate that TFM is susceptible to both anaerobic and aerobic microbial degradation,19,18,23,28−30 the effect of microbial processes on niclosamide fate is not well understood.26,31,32 A limited number of studies indicate that both TFM and niclosamide undergo pH-dependent photolysis under environmentally relevant conditions.2,13,14,19,21,27,33 Although several organic and inorganic products have been identified during the photodegradation of TFM and niclosamide, the photolysis rates of both lampricides under natural conditions have not been adequately characterized. Mechanistic details would benefit our understanding of the fate of these compounds and their transformation products in natural environments. Additionally, although the two lampricides are often used in tandem to target the sea lamprey, they have not been studied under the same irradiation conditions, making it difficult to compare photolysis rates to one another or to previously reported rates. The objective of this work was to determine the direct photodegradation rates and pathways of TFM and niclosamide. To this end, we evaluated the impact of pH on photolysis rates and used this data to calculate the quantum yield and half-life of these compounds under environmentally relevant conditions. Furthermore, we investigated the photodegradation pathways of the two compounds to form organic and inorganic products and incorporated these results into kinetic models. These results allow us to better predict the rate of direct photolysis of the lampricides in surface waters, which can benefit sea lamprey management efforts and may help reduce unintended impacts to nontarget species. B


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Environmental Science & Technology

Figure 1. (a) Direct photodegradation rates and (b) quantum yields of 10 μM TFM and 1 μM niclosamide as a function of pH. (c) Comparison of the molar extinction coefficients of TFM and niclosamide (pH 8) and modeled solar irradiance for Madison, WI, at noon on August 1, 2015. (d) Concentrations of TFM, GA, TFA, 4OHCat, and MA during the photolysis of TFM (symbols; pH 8). Lines represent modeled kinetic data. The line titled, ∑ Unknowns, represents the unaccounted for carbon mass that is not described by Scheme 1. Concentrations of (e) TFM, TFA, fluoride, total F species and (f) nitrate, nitrite, and total N species generated during the photolysis of TFM (pH 8). Total F species refers to the sum of [TFM], [TFA], and [F−]. Total N species refers to the sum of [TFM], [NO2−], and [NO3−]. The solid lines represent the expected material balance of (e) [F−] (eq S13) and (f) ([NO3−] + [NO2−] (eq S11) assuming complete dehalogenation and denitrogenation of all organic compounds.

The ultraviolet−visible (UV−vis) absorbance spectrum and pH of each water sample and the chemical actinometer were analyzed prior to and following irradiation using a Shimadzu UV2401PC UV−vis spectrophotometer and a Mettler Toledo EL20 portable pH meter, respectively. The acid dissociation constants (pKa) of TFM and niclosamide were determined spectrophotometrically (Section S7). A full scan LC-MS/MS method was conducted using both positive and negative electrospray ionization to identify the mass

niclosamide. Samples were irradiated until at least half of each lampricide was degraded. Subsequent photolysis experiments using the lampricides and proposed intermediates were conducted only at pH 8, which falls within the typical pH range of Great Lakes tributaries (i.e., 7.4−8.5).36 Analytical Methods. The two lampricides, six aromatic intermediates, maleic acid, and trifluoroacetic acid were quantified by HPLC or liquid chromatography-tandem mass spectrometry (LC-MS/MS; Section S5). C


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Table 1. Direct Photodegradation Rate (Corrected for Light Screening) and Quantum Yield of 10 μM TFM, Niclosamide, Proposed Aromatic Intermediates, and Maleic Acid Determined at pH 8 Using 365 nm Fixed-Wavelength Bulbsa sunlight t1/2 (h) −1

compound name

kdirect (min )

Φ365

surface

55 cm depth

3-trifluoromethyl-4-nitrophenol (TFM) 2′,5-dichloro-4′-nitrosalicylanilide (niclosamide; NIC) 5-chlorosalicylic acid (5ClSA) 2,5-dihydroxybenzoic acid (gentisic acid; GA) 2-chloro-4-nitroaniline (2Cl4NA) 2-chloro-4-nitrophenol (2Cl4NP) 4-nitrocatechol (4NCat) 1,2,4-benzenetriol (4-hydroxycatechol; 4OHCat) maleic acid (MA)

(1.24 ± 0.06) × 10−2 (2.24 ± 0.05) × 10−4 (5.35 ± 0.04) × 10−2 (6.21 ± 0.03) × 10−3 (4.02 ± 0.05) × 10−3 (1.06 ± 0.03) × 10−3 (5.35 ± 0.11) × 10−3 (4.08 ± 0.18) × 10−2 (2.64 ± 0.11) × 10−4

(2.03 ± 0.09) × 10−4 (1.18 ± 0.03) × 10−6 (2.86 ± 0.02) × 10−1 (1.53 ± 0.01) × 10−3 (1.57 ± 0.02) × 10−5 (6.06 ± 0.17) × 10−6 (5.35 ± 0.11) × 10−3 (1.08 ± 0.05) × 10−3 (9.90 ± 0.42) × 10−3

1.64 ± 0.08 254 ± 6 0.076 ± 0.001 2.67 ± 0.01 26.3 ± 0.3 37.4 ± 1.1 6.48 ± 0.14 1.12 ± 0.05 123 ± 5

19.6 ± 0.9 3,040 ± 70 0.904 ± 0.007 31.9 ± 0.2 315 ± 4 448 ± 13 77.6 ± 1.7 13.4 ± 0.6 1,480 ± 70

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The experimentally derived quantum yield and modeled sunlight intensity data [SMARTS: Madison, WI (43.0667° N, 89.4000°W), noon, August 1, 2015] were used to calculate the half-life of each compound at the surface of the water column and over an average depth of 55 cm, assuming continuous noontime irradiation.

S10). Finally, material balance calculations were used to estimate expected organic and inorganic concentrations formed during the photodegradation of TFM and niclosamide (Section S9).

to charge (m/z) ratios of ionizable unknown compounds formed throughout the course of irradiation of the lampricides and proposed intermediates (i.e., 2Cl4NA, 2Cl4NP, 4NCat, 4OHCat, 5ClSA, and GA; Section S8). Samples were collected prior to, midway through, and following sample irradiation to assess the potential formation of additional organic photoproducts. The concentrations of chloride (Cl−), fluoride (F−), nitrate (NO3−), and nitrite (NO2−) formed during the photolysis of the lampricides were quantified by ion chromatography (Section S5). Calculations and Modeling. The photodegradation rates of TFM, niclosamide, and proposed intermediates were calculated by fitting the data assuming first-order kinetics. All observed rate constants (kobs) determined from experimental data were corrected for light screening, yielding the direct photodegradation rate (kdirect; Section S9).37 Error bars represent the standard deviation of triplicate analyses. The direct quantum yield (Φunk) of each compound was calculated according to:34,37 Φunk =

kobs,unk kabs,act · ·Φact kobs,act kabs,unk

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RESULTS AND DISCUSSION Effect of pH on Direct Photolysis Rates. Solution pH impacts the direct photodegradation rate and quantum yield of TFM. The rate of TFM photodegradation increases with increasing pH values (Figure 1a; Table S3). For example, the rate of TFM photolysis under experimental conditions is (3.88 ± 0.05) × 10−3 min−1 at pH 4 and (1.45 ± 0.02) × 10−2 min−1 at pH 9. The higher photolysis rate of TFM under alkaline conditions is consistent with previous studies.2,21 The trend between the direct photolysis quantum yield of TFM and pH is less clear and does not follow a species-based model.40 Although the quantum yield of TFM appears to decrease with increasing pH values (i.e., from 3.15 × 10−4 at pH 4 to 2.17 × 10−4 at pH 9), this trend does not explain the pH dependence of the direct photolysis rate. Instead, the pH dependence is primarily correlated with an increase in light absorption as the lampricide becomes deprotonated at higher pH values (pKa = 6.38 ± 0.02; Figures S5a,b and S14). Experimentally determined photolysis rate constants were used to predict TFM loss rates at the surface of the water column and integrated over a depth of 55 cm (eqs S9 and S10; Table S3). The quantum yield and predicted half-life of TFM reported here agree with previously published data.22 The quantum yield calculated in this study was (1.13 ± 0.03) × 10−4 at pH 7, resulting in a predicted half-life of 3.01 ± 0.09 h (continuous irradiation by sunlight at the surface of the water column) and 36.1 ± 1.0 h (continuous irradiation integrated over 55 cm of the water column). Similarly, Carey and Fox22 reported a TFM quantum yield of (1.3 ± 0.5) × 10−4 at pH 7 using 360 nm fixedwavelength bulbs, which corresponded to a half-life of 36 h assuming continuous irradiation by sunlight over a depth of 55 cm. The direct photodegradation rates, quantum yield, and halflife predictions of TFM at other pH values presented in Table S3 have not been previously reported. Both the photodegradation rate and quantum yield of niclosamide decrease with increasing pH. The rate of direct photolysis of niclosamide ranges 2 orders of magnitude from (1.60 ± 0.15) × 10−3 min−1 at pH 5 to (6.79 ± 1.21) × 10−5 min−1 at pH 9 under our experimental conditions (Figure 1a; Figure S12). Although niclosamide exhibits greater light absorption under more alkaline conditions (pKa = 6.02 ± 0.14;

(1)

where kobs is the observed photodegradation rate of the target compound (unk) or the actinometer (act) assuming first-order kinetics, kabs is the rate of light absorption of the target compound or the actinometer (described in Section S9), and Φact is the quantum yield of the actinometer.34,35,37 The “Simple Model of the Atmospheric Radiative Transfer of Sunshine” (SMARTS) was used to model the spectral properties of natural sunlight irradiance for Madison, WI, at noon on August 1, 2015 (Section S3).38 The global horizontal irradiance generated by SMARTS was combined with our UV−vis data to calculate kabs for both compounds under sunlight irradiation. These data were combined with the experimentally derived quantum yield data to predict the half-life of TFM and niclosamide exposed to natural sunlight at the surface of the water column and integrated over a depth of 55 cm (Section S9). This depth was chosen to enable direct comparison with a previous study22 in order to validate our experimental approach and calculations. Kintecus simulation software39 was used to model the photodegradation kinetics of the lampricides and known photoproducts using experimentally determined rates (Section D


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Despite the increase in TFA throughout the irradiation, the resulting concentration was low (302 ± 3 nM after 400 min of irradiation). After 400 min of photolysis, the sum of TFM, GA, 4OHCat, and MA remaining in solution was 0.76 ± 0.04 μM. Therefore, the carbon material balance declined from 47.5% after 95 min to 8.0% after 400 min, demonstrating that TFM and its organic intermediates form additional unidentified photoproducts (described below). Furthermore, no other significant peaks were detected using our HPLC method with UV−vis detection from 200 to 500 nm, which was designed to retain MA and provide optimal separation for the relatively polar aromatic photolysis products (Scheme 1), indicating that additional photostable organic products likely lack conjugated double bonds and may therefore be ring cleavage products. A kinetic model of TFM photodegradation was constructed according to the proposed reaction pathway using the direct photolysis rates of each intermediate photoproduct. The direct photodegradation of each compound followed first-order kinetics, with rates varying over 2 orders of magnitude (Table 1). 4OHCat degrades approximately four times more rapidly (kdirect = (4.08 ± 0.18) × 10−2 min−1) than TFM (kdirect = (1.24 ± 0.06) × 10−2 min−1) and therefore is not expected to build up in solution. In contrast, GA and MA are less photolabile than TFM and thus are expected to accumulate in solution. The kinetic model was initially designed assuming 100% conversion from one product to the next following the outlined pathway (Scheme 1). Experimental data was subsequently used to tune the kinetic model. For example, if we assumed that all TFM in solution degrades to GA (100% conversion), based on the direct photodegradation rate of GA, we estimate that the direct photodegradation of 10 μM TFM should yield 5.51 μM GA. Instead, experimental data indicate that a maximum 1.69 μM GA is formed, corresponding to a 33% conversion (Figure 1d; Section S11). Note that this approach assumes that the photonucleophilic substitution of TFM is the rate-limiting step in GA formation and that any additional intermediates (i.e., trifluoromethylhydroquinone) are unstable and undergo rapid photolysis.13,22 Following this approach, the percent yield of each subsequent product was allocated using experimental data (Scheme 1; Figures S7 and S11). Modeled results demonstrate three key characteristics of TFM photodegradation. First, the analysis allowed us to quantify the yield of GA, confirming that the compound is a major photoproduct of TFM photolysis.13,19,22 Second, the low yield of TFA (3.2%; pH 8) is consistent with TFA yields detected previously (2−7%; pH 7−9).13 Finally, the model illustrates that the identified products do not account for the complete carbon material balance, suggesting that other intermediates are formed during the photolysis of TFM (represented as “∑ Unknowns” in Figure 1d). Niclosamide Photodegradation Pathway. The niclosamide photodegradation pathway (Scheme 1) was constructed by conducting individual direct photodegradation studies with each proposed aromatic intermediate. For example, direct photolysis of 4NCat led to the formation of 4OHCat and MA, while direct photolysis of 5ClSA led to the formation of GA, 4OHCat, and MA (Figures S6−S11). These results confirm the previously proposed mechanism in which niclosamide undergoes cleavage at the amide bond to form 2Cl4NA and 5ClSA.2 Furthermore, this study extends the mechanism by identifying multiple intermediate products and establishing the order in which products are formed. Our analysis demonstrates that the aromatic intermediates undergo photolysis and lose their

Figure S5c,d), the trend with pH is more strongly influenced by the quantum yield of niclosamide, which correspondingly increases with decreasing pH from (3.21 ± 0.57) × 10−6 at pH 9 to (1.62 ± 0.15) × 10−4 at pH 5 (Figure 1b; Figure S15). Nearly identical quantum yields of 1.6 × 10−6 and 1.2 × 10−4 were determined at pH 9 and 5, respectively, using 450 W xenon bulbs (Section S6). The agreement between the quantum yields measured using both light sources suggests that the data determined using the fixed-wavelength bulbs is representative of actinic irradiation for this compound, likely because niclosamide absorbs strongly at 365 nm (Figure 1c). The experimental quantum yields were used to predict the rates of niclosamide photolysis in sunlight. The predicted halflives of 1 μM niclosamide are 19.8 ± 2.0 h at pH 5, 35.5 ± 1.4 h at pH 7, and 765 ± 166 h at pH 9 assuming continuous irradiation at the surface of the water column (Table S4). These half-lives are at least three times longer than previously reported values. Graebing et al.2 reported direct photolysis half-lives of niclosamide of 6.80 h at pH 5 (initial concentration =0.15 μM), 10.7 h at pH 7 (initial concentration =1.4 μM), and 29.5 h at pH 9 (initial concentration =7.3 μM) using an Heraeus Suntest CPS photounit, designed to closely match solar radiation. The reason for this discrepancy is unclear. This is the first study to evaluate the photolysis of TFM and niclosamide under the same irradiation conditions, allowing for direct comparison of the photolysis rates of the lampricides. Although both compounds absorb light within the solar spectrum (Figure 1c; absorption maxima of ε395 = 1.61 × 104 M−1 cm−1 for TFM and ε375 = 1.42 × 104 M−1 cm−1 for niclosamide, pH 8), the two compounds have opposite trends in photodegradation rates with pH due to differences in quantum yields (Figure 1b, Tables S3 and S4). At pH 8, the quantum yield of TFM is 2 orders of magnitude greater than niclosamide (Table 1). As a result, the predicted half-life of TFM at the surface of the water column (i.e., 1.64 ± 0.08 h) is 2 orders of magnitude shorter than niclosamide (i.e., 254 ± 6 h). At pH 7, the quantum yields are nearly identical (Figure 1b, Tables S3 and S4), but the photolysis rate of TFM is still an order of magnitude greater than niclosamide due to the higher rate of TFM light absorbance. TFM Photodegradation Pathway. The proposed TFM degradation pathway (Scheme 1) was constructed by conducting individual direct photodegradation studies with GA, 4OHCat, and MA (Table 1). These experiments demonstrate that GA degrades to 4OHCat, and 4OHCat degrades to MA (Figures S7 and S11). Direct photodegradation experiments were not conducted with TFA, which is not susceptible to photolysis.13 The proposed pathway builds on previous studies which demonstrated that the major TFM photodegradation pathway involves photonucleophilic substitution of the nitro group by a hydroxyl group to produce trifluoromethylhydroquinone.22 Trifluoromethylhydroquinone may then photodegrade to either trifluoromethylquinone or an acid fluoride (i.e., 2,5-dihydroxybenzoyl fluoride), leading to GA19,22 and TFA,13 respectively. Our study focused on the more stable known photoproducts (i.e., GA and TFA) rather than the hydroquinone, as these are more likely to persist in the environment. In addition, the identification of 4OHCat and MA as photoproducts of TFM is novel. We then determined the carbon material balance using TFM and its quantified photoproducts according to eq S11. Irradiating 9.51 μM TFM (pH 8) for 95 min resulted in 2.31 ± 0.08 μM TFM and the formation of 1.69 ± 0.04 μM GA, 0.04 ± 0.01 μM TFA, and 0.47 ± 0.06 μM 4OHCat (Figure 1d; Figure S13). E


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Figure 2. (a) Concentrations of niclosamide, 5ClSA, GA, 2Cl4NA, 2Cl4NP, 4NCat, 4OHCat, and MA during the photolysis of niclosamide (symbols; pH 8). Lines represent modeled kinetic data. Panel (b) is an expanded version of panel (a). Concentrations of (c) niclosamide, chloride, sum of Cl containing aromatics, total Cl species and (d) nitrate, nitrite, sum of N containing aromatics, and total N species present during the photolysis of niclosamide (pH 8). Total Cl species refers to the sum of [niclosamide], [2Cl4NA], [2Cl4NP], [5ClSA], and [Cl−]. Total N species refers to the sum of [niclosamide], [2Cl4NA], [2Cl4NP], [4NCat], [NO2−], and [NO3−]. The solid lines represent the expected material balance of (c) [Cl−] (eq S12) and (d) ([NO3−] + [NO2−]; eq S11), assuming complete dehalogenation and denitrogenation of all organic compounds.

magnitude, which affects the quantity of each product formed. For example, comparing the first two products formed after the cleavage of the amide bond in niclosamide, 5ClSA forms and then rapidly degrades, while 2Cl4NA is more persistent due to its slower direct photolysis rate (Table 1). This observation explains why a previous study detected 2Cl4NA but not 5ClSA.2 Generally, modeled and experimental data align closely with a few key exceptions. During the direct photodegradation of 2Cl4NA, the model underpredicts the formation 4OHCat or MA compared to experimental data (Figure S8). Similarly, the model underpredicts the formation of MA from 2Cl4NP (Figure S9) and 4NCat (Figure S10). These findings suggest that other intermediate species are formed which subsequently degrade to 4OHCat and MA. The absence of additional HPLC-UV peaks indicates that these intermediates are highly photolabile. The niclosamide kinetic model demonstrates four key points. First, the initial photolysis of niclosamide is much slower than the direct photodegradation of the products (Table 1) and therefore is the rate-limiting step in its transformation. Second, the concentrations of aromatic intermediates and MA are always less than 10% of the initial niclosamide concentration due to their relatively rapid photolysis and therefore do not accumulate in solution. Third, TFM and niclosamide share several degradation

subsituents in order of increasing electronegativity (e.g., 2Cl4NA loses the amino group, followed by the chloro group, followed by the nitro group). Six aromatic compounds and MA were formed during the photodegradation of niclosamide (Figures 2a,b). As observed for TFM, no other major peaks were detected by HPLC-UV during niclosamide photolysis; therefore, it is likely that additional photostable products lack conjugated double bonds and may be ring cleavage products. Despite the formation of all of the compounds in the proposed pathway (Scheme 1), none were detected above 0.3 μM ([niclosamide]t=0 = 9.78 μM) over the 144 h photolysis. Only two of these photoproducts (i.e., 2Cl4NA and MA) were previously detected at similarly low concentrations.2 Niclosamide, the six aromatic intermediates, and maleic acid accounted for 56.2% of the carbon material balance after 26.4 h of irradiation and 10.8% after 144 h of irradiation (eq S12). A kinetic model for niclosamide photolysis was constructed according to Scheme 1. Due to their relatively rapid direct photolysis rates compared to niclosamide (Table 1), the intermediate products (with the exception of maleic acid) do not accumulate in solution (Figure 2a,b). The photolysis rates of the aromatic photoproducts differ by at least an order of F


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Formation of Inorganic Products. Because our reaction pathway indicates that the aromatic intermediates produced by TFM and niclosamide undergo dehalogenation and denitrogenation, we investigated the formation of inorganic ions during lampricide photolysis. Complete dehalogenation and denitrogenation of 10 μM TFM and its organic photoproducts would produce 30 μM fluoride and 10 μM of nitrate/nitrite (eqs S11 and S13). Since nitrite can be oxidized to nitrate in the presence of oxygen (i.e., under our experimental conditions), we summed the concentrations of both oxyanions for the purpose of calculating the material balance on nitrogen containing species (Figure 1e,f). After 400 min of irradiation, 75.7 ± 1.4% of TFM is converted to fluoride, while 13.4 ± 0.1% is converted to nitrate/ nitrite (pH 8; eqs S14 and S15). Our data is consistent with previous studies which demonstrated that 75% (pH 9.2) of TFM was converted to fluoride and 55% (pH 7) of TFM was converted to nitrite during TFM photolysis.13,22,23 The photoproduction of fluoride and nitrate/nitrite indicates that significant degradation of TFM has occurred. Trifluoromethyl and nitro groups are both highly electronegative (EN = 3.4 for −CF3 and −NO2 on the Pauling scale)41 and are difficult to oxidize. Therefore, it is likely that additional fluoro- and nitrocontaining organic species (i.e., intermediate photoproducts) are still present in solution after the parent compound has degraded. For example, nine of the 24 unknown compounds produced during TFM photolysis contain one N atom according to the nitrogen rule (Table S5). Additionally, a fraction of TFM (3.2%; pH 8) degrades to trifluoroacetic acid13 (Figures 1d,e), illustrating that TFM produces smaller fluorine-containing organic molecules during photolysis. Unknowns containing fluorine and nitrogen could not be included in the material balance calculation and likely account for the disparity in the material balance. Similarly, the photolysis of niclosamide produces chloride and nitrate/nitrite as inorganic products. Complete dehalogenation and denitrogenation of 10 μM niclosamide and the resulting aromatic intermediates would produce 20 μM of chloride and 10 μM of nitrate and/or nitrite (Figures 2c,d, eqs S11 and S12). After 144 h of photolysis, 88.0 ± 2.3% of niclosamide is converted to chloride, while 46.7 ± 3.2% is converted to nitrate/ nitrite (pH8; eqs S15 and S16). The formation of chloride and nitrate/nitrite during niclosamide photolysis has not been previously reported. Nitro groups are more electronegative than chloro groups (EN = 3.4 and 3.0, respectively, on the Pauling scale)41 and are therefore more difficult to oxidize. Of the seven quantified products and 37 unknowns produced by niclosamide photolysis, 41% contain one N atom and 38% contain Cl as interpreted from the mass spectra (Table S6). Therefore, additional nitro- and chloro-containing organic species are likely still present in solution. Furthermore, previous work has shown that niclosamide mineralization occurs during photolysis, leading to approximately 40% mineralization to carbon dioxide after long irradiation durations.2,19 Collectively, the generation of these inorganic species in solution during photolysis indicates that substantial degradation of niclosamide and the resulting organic intermediate photoproducts has occurred.

products including GA, 4OHCat, and MA. Fourth, in addition to the outlined pathway, 4OHCat and MA are likely formed during the photolysis of unknown photolabile intermediates. Formation of Organic Unknowns. To investigate the formation of additional unknown photoproducts, TFM and niclosamide photolysis samples were analyzed by LC-MS/MS using both negative and positive electrospray ionization (Section S8). It is important to note that this approach only detects products that are amenable to ionization by electrospray and that the ion abundance depends on the response of each compound to the ionization technique. Using this approach, the m/z values of 15 compounds unique to TFM photodegradation (lettered; Table S5), nine compounds common to both TFM and niclosamide photodegradation (numbered; Table S5), and 28 compounds unique to niclosamide photodegradation (numbered; Table S6) were identified. All of these compounds have unique retention times, and many have proposed masses that are consistent with compounds containing three, four, or five carbons with amino-, chloro-, fluoro-, and/or nitro-groups (i.e., possible ring cleavage products of TFM, niclosamide, or the aromatic intermediates). For example, nine and 15 of the products of TFM and niclosamide, respectively, contain one N atom and 14 of the products of niclosamide contain one Cl atom (Tables S5 and S6). Twenty-four unidentified species with unique m/z values were formed during the photolysis of TFM (Table S5). Four of the m/ z values correspond to photoproducts proposed by Hubert.19 These include 3-trifluoromethyl-4-nitrosophenol (Hubert A), 3trifluorormethyl-5-nitroso-1,4-benzenediol (Hubert C), 3-trifluoromethyl-5-nitro-1,4-benzenediol (Hubert D), and 2,5-diolbenzoyl fluoride (Hubert G). The m/z value of 3-trifluoromethyl-4-nitrosophenol (Hubert A) was present as a sodium adduct at 68% of the total expected abundance when 99.9% of TFM had been degraded, suggesting that this compound may be an important intermediate in the degradation of TFM. Authentic standards were not available to confirm compound identity. The m/z values of 37 unknown species were identified as niclosamide photoproducts (Table S6). Nine of these unknown photoproducts were generated by both TFM and niclosamide (i.e., the same m/z and the same retention time; Table S5−S6). Since TFM and niclosamide share several intermediate photoproducts (i.e., GA, 4OHCat, and MA), the possibility of sharing additional degradation products is likely. Of these nine unknowns, two contain nitrogen atoms and five are associated with potential formulas based on likely ring cleavage products (i.e., with four or five carbon atoms). Finally, to gain additional information about the origin of the unknown products, we examined whether any unknowns are produced during the direct photodegradation of the aromatic intermediates (5ClSA, GA, 2Cl4NA, 2Cl4NP, 4NCat, 4OHCat; Table S7). This analysis illustrates that of the 24 unknown m/z ratios identified during TFM photodegradation, 13 are present during the photolysis of one or more of the aromatic intermediates (Section S13). Of the 37 unknown m/z ratios identified during niclosamide photodegradation, 20 are present during the photolysis of one or more of the aromatic intermediates. These results demonstrate that many of the unknown compounds likely originate from the photolysis of the identified aromatic intermediates. In summary, this analysis demonstrates that the photolysis of TFM and niclosamide leads to the production of numerous different compounds, many of which appear to be ring cleavage products.

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ENVIRONMENTAL IMPLICATIONS Determining the rates and pathways of lampricide photodegradation improves our understanding of their environmental fate. Both compounds are applied directly to tributaries of the Great Lakes, where they are exposed to sunlight. The residence G



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time of TFM and niclosamide in tributaries during lampricide applications is on the order of hours to several days depending on the tributary itself, the hydrologic conditions, and the location of sea lamprey larvae.22 Our predicted photolysis half-life of TFM ranges from 16.6 to 32.9 h over the pH range 6 to 9, while the half-life of niclosamide ranges from 8.88 to 382 days over the same pH range (assuming continuous noontime irradiation over a water depth of 55 cm). In tributaries where lampricides are applied, sunlight exposure will be subject to annual variability, diurnal fluctuations, cloud cover, and canopy cover, impacting the degradation rate. Therefore, these half-lives represent the shortest expected lifetimes based on ideal irradiation conditions. While sorption is not expected to play a significant role in the fate of TFM (organic carbon partition coefficient (Koc) = 129− 14.2; pH 6−9),16,19 sorption is expected to contribute to the fate of niclosamide in natural systems (Koc = 3111 ± 1552; pH 7.4).26 Furthermore, although additional niclosamide biodegradation studies are needed,32,42 the estimated biodegradation half-lives of TFM (5.5 days, aerobic)28 2.1 days, anaerobic29 ) and niclosamide (1.1−3.9 days, aerobic26) indicate that microbial processes may influence lampricide fate in the tributaries where they are applied. Given these half-lives and the residence time of lampricides in tributaries during their application, it is likely that both biodegradation and phototransformation of TFM will occur during a dosing event. This agrees with a previous observation of TFM photodegradation during a lampricide application.27 In contrast, we hypothesize that direct photodegradation of niclosamide within tributaries of the Great Lakes will be minimal. Ongoing studies will examine the impact of dissolved organic matter (DOM) on the rates of photolysis of the lampricides because the presence of DOM could either increase or decrease the rates.43,44 Finally, although niclosamide is added in much smaller quantities than TFM, it is less selective for the sea lamprey and is photochemically more persistent. The slow photolysis of niclosamide demonstrated in this work suggests that the risk of adverse effects to nontarget organisms following niclosamide applications may be a concern. Unlike other chemicals which inadvertently reach the Great Lakes including PCBs, mercury, and trace organic compounds (e.g., pesticides and personal care products),43,45−47 known quantities of TFM and niclosamide are purposefully added to Great Lakes tributaries. Examining the photodegradation of TFM and niclosamide has implications for other halogenated aromatic phenolic compounds. For example, photodehalogenation has been shown to occur for bromofenoxim,48 2bromophenol,49 2-chlorophenol,50 triclosan,51−53 2,4-dichlorophenol,50,51,53 and several hydroxylated diphenyl ethers.54 Our study demonstrates that exposure to sunlight can lead to ring cleavage, dehalogenation, and denitrogenation of lampricides. Our work also demonstrates that niclosamide degradation is the rate-limiting step toward eventual mineralization. Generally, hydroxylation of aromatic rings, loss of halogen moieties, and loss of aromaticity results in less persistent and more biodegradable compounds.18,55

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Article

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Telephone: (608) 262-1820. Fax: (608) 262-0454. Twitter: @remucal. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors thank Laura Linde for her contribution to this work. We thank Jane Rivera (USGS Upper Midwest Environmental Science Center) for her assistance with QA/QC. Funding for this study was provided by the Wisconsin Sea Grant, the Great Lakes Fishery Commission, and a National Science Foundation Graduate Research Fellowship (awarded to M.M.B.). Any use of trade, product, or firm names is for descriptive purposes and does not imply endorsement by the U.S. Government.

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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.est.6b02607. Additional experimental details, Figures S1−S15, and Tables S1−S7. Raw data for this study is archived at https://minds.wisconsin.edu/. (PDF) H


Article

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