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Bifenthrin Causes Trophic Cascade and Altered Insect Emergence in Mesocosms: Implications for Small Streams Holly A. Rogers,† Travis S. Schmidt,*,†,‡ Brittanie L. Dabney,†,§ Michelle L. Hladik,∥ Barbara J. Mahler,⊥ and Peter C. Van Metre⊥ †

U.S. Geological Survey, Fort Collins Science Center, 2150 Centre Avenue, Bldg. C, Fort Collins, Colorado 80526, United States U.S. Geological Survey, Colorado Water Science Center, Lakewood, Colorado 80225, United States § Department of Fish, Wildlife, and Conservation Biology, Colorado State University, Fort Collins, Colorado 80523, United States ∥ U.S. Geological Survey, California Water Science Center, Sacramento, California 95819, United States ⊥ U.S. Geological Survey, Texas Water Science Center, Austin, Texas 78754, United States ‡

S Supporting Information *

ABSTRACT: Direct and indirect ecological effects of the widely used insecticide bifenthrin on stream ecosystems are largely unknown. To investigate such effects, a manipulative experiment was conducted in stream mesocosms that were colonized by aquatic insect communities and exposed to bifenthrin-contaminated sediment; implications for natural streams were interpreted through comparison of mesocosm results to a survey of 100 Midwestern streams, USA. In the mesocosm experiment, direct effects of bifenthrin exposure included reduced larval macroinvertebrate abundance, richness, and biomass at concentrations (EC50’s ranged from 197.6 to 233.5 ng bifenthrin/g organic carbon) previously thought safe for aquatic life. Indirect effects included a trophic cascade in which periphyton abundance increased after macroinvertebrate scrapers decreased. Adult emergence dynamics and corresponding terrestrial subsidies were altered at all bifenthrin concentrations tested. Extrapolating these results to the Midwestern stream assessment suggests pervasive ecological effects, with altered emergence dynamics likely in 40% of streams and a trophic cascade in 7% of streams. This study provides new evidence that a common pyrethroid might alter aquatic and terrestrial ecosystem function at the regional scale.

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high as 23.9 μg bifenthrin/g organic carbon (OC) have been measured in stream sediment.8 Pyrethroid occurrence in aquatic ecosystems is so pervasive in the United States that at least one nontarget freshwater organism (Hyalella azteca) has evolved resistance in some affected populations.9 Although there have been surveys characterizing the extent of pyrethroid contamination in surface waters and stream sediments in the United States,7,8,10,11 observational studies (e.g., bioassessment surveys) that relate pyrethroid exposure to changes in ecological communities are rare.12,13 Most pesticide monitoring programs document environmental concentrations of pesticides7,8,10,11,13 and measure or estimate effects with short-term, single-species toxicity tests such as the Hyalella azteca test or the Chironomus tests.14−17 These tests are viewed as reliable assessment tools in part because they may establish causation and are more replicable and less variable than field observations, but test conditions do

INTRODUCTION Global agricultural chemical use is increasing in order to improve crop yields as arable land declines.1 Urban use of pesticides also is increasing, partly as a means to mitigate the spread of disease (e.g., Zika, Dengue) vectors.1,2 As a result, pesticides are now agents of global ecological change. In global surveys, regional freshwater biodiversity was decreased in areas where pesticides were used,3 and pesticides, especially pyrethroids, were detected above regulatory thresholds at a greater frequency than expected.2 These findings are mostly restricted to developed countries where, over the past 20 years, growth in the use of pyrethroids has been driven by the need to replace organophosphate insecticides.4 Future market growth is likely in developing countries,5 increasing the global extent to which pyrethroids are found in freshwater ecosystems. Bifenthrin is a pyrethroid insecticide commonly used in both residential and agricultural settings, and because it is hydrophobic (log Kow ∼ 6) and insoluble in water and has a relatively long half-life (8−17 months6) in sediment, bifenthrin can persist in stream sediments longer than in the water column. A survey across the continental United States detected bifenthrin in 58% of the streams (n = 36) sampled.7 Concentrations as This article not subject to U.S. Copyright. Published XXXX by the American Chemical Society

Received: June 2, 2016 Revised: September 8, 2016 Accepted: September 21, 2016

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DOI: 10.1021/acs.est.6b02761 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Environmental Science & Technology

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5.7 L of river water and equipped with a pump to recirculate the water and simulate a riffle environment. Peristaltic pumps continuously delivered river water to the mesocosms for one daily volume replacement. Mesocosms were kept in a water bath to maintain temperature (13.8 °C) comparable to that of the Poudre River at the time of tray retrieval. Sediment Spikes. Sediment exposures were used in this test because bifenthrin partitions to sediments and therefore often is transported to streams adsorbed to fine particles.11,13 Nominal bifenthrin concentrations for the sediment spikes were 0.63, 1.25, 2.5, 5.0, 10.0, and 20.0 μg/g dry weight (dw), replicated in triplicate with four controls (n = 22 mesocosm streams). Concentrations were chosen on the basis of a pilot study that showed high macroinvertebrate mortality at 20 and 200 μg/g dw. For the exposures, 285 mg of dry Poudre River fine sediment (Figure S1C, 98% purity, Chem Service, West Chester, Pennsylvania; spectrophotometric grade acetone, Sigma-Aldrich, St. Louis, Missouri). Acetone was added to all spikes (including bifenthrin-free control sediment spikes) to a final volume of 20 mL and allowed to evaporate. Spikes were stored in 50 mL of Poudre River water for 4 days at approximately 6 °C to equilibrate. All mesocosms received a single spike at the beginning of the test to simulate one runoff event. The 285 mg of spiked sediment comprised a very small portion of the total bulk sediment in each mesocosm at the time of spike delivery (Figure S1C). Bifenthrin concentrations were measured in the initial spikes (one split per treatment) and the bulk sediment collected from each mesocosm upon termination of the experiment (day 30) (see Bulk Sediment Collection and Analytical Chemistry). A “time zero” bulk sediment concentration could not be estimated without compromising the mesocosms. We also measured concentrations of bifenthrin lost from the sediment spike to other phases (i.e., dissolved, particulate, and adsorbed to the walls of the mesocosm container) during this test and during a pilot study (see SI section 2, Table S1−S2). Water-Sample Collection. To determine the fate of bifenthrin added to the mesocosms, whole (unfiltered) and dissolved water samples were analyzed at a range of times after the spiked sediment addition. About 333 mL of water was removed from each of the three replicate mesocosms (250 mL from four controls) 5−10 min after exposure and composited into a 1 L amber glass bottle. Excluding the controls, additional samples were collected 24, 48, and 96 h after spike addition. Samples were analyzed as described in Analytical Chemistry. Following detections above the detection limit in the dissolved and/or whole water phases, additional samples were collected from mesocosms exposed to the three highest bifenthrin concentrations on day 8 and from mesocosms exposed to the two highest concentrations on day 16 (Tables S2 and S3). Because no dissolved bifenthrin was detected on day 16, no additional water samples were collected (Table S3). Water temperature, pH, and specific conductivity were measured in each mesocosm biweekly (Hach HQ40d, Loveland, Colorado). Invertebrate and Periphyton Collection. Emergent adults were aspirated daily from nets covering each mesocosm. Adults were sexed and identified to genus, except for Chironomidae, which were identified to subfamily or tribe.29 Adults were composited by family (either Chironomidae or Baetidae) for each treatment (n = 14), freeze-dried, weighed, and analyzed

not reflect the complex conditions in ecosystems. In most cases, the Hyalella azteca test is used to expose crustaceans to acutely toxic levels of pesticides, lasts for 10 days, is conducted at 25 °C, and documents only direct effects (e.g., mortality, growth) of contaminants on crustaceans. However, in most aquatic ecosystems, insects, not crustaceans, are the most numerically dominant and diverse group of organisms, and they typically are exposed to subacutely toxic concentrations of contaminants for more than 10 days18 and at temperatures below 25 °C.10 At least one study has questioned the utility of standard toxicity tests for describing aquatic insect responses to pyrethroids.19 Although more environmentally relevant than bioassays, field studies are limited in their ability to causally link ecological responses to a particular stressor because natural streams commonly are affected by multiple contaminants or stressors (e.g., pesticides, sediment load, flow alteration).20 Mesocosm studies can bridge the credibility gap between overly simplified standard laboratory toxicity tests and the complexity of natural ecosystems.20 Mesocosm studies can establish causal relationships between a contaminant and ecological responses, create more realistic exposure scenarios (e.g., simultaneous water, food, and sediment exposure, 30 day exposure duration) than observed in standard toxicity-testing scenarios, and create opportunities for long-lived aquatic insects to experience a sensitive life event (e.g., molting, metamorphosis).20−24 Mesocosm studies also allow manipulation of a known stressor or stressors over a controlled range of levels. Mesocosm tests with natural communities expose many species to contaminants simultaneously, thus offering the opportunity to observe indirect effects (e.g., trophic cascades, interspecies interactions, subsidies) of contaminants on ecosystems.25 Such contaminant-related indirect effects might be as or more important to ecosystems than direct effects such as mortality.26 We conducted an experiment that simulated a single runoff event delivering bifenthrin adsorbed to suspended sediments to mesocosm streams. This type of runoff event is the most likely transport mechanism of bifenthrin to receiving streams and thus a likely exposure scenario for stream invertebrates.13 This experiment accompanied a regional assessment of contaminants and ecological communities in 100 streams across the Midwestern USA (http://txpub.usgs.gov/RSQA/). The purpose of the mesocosm experiment was to assess the direct and indirect effects of sediment-bound bifenthrin on natural aquatic communities under controlled conditions and compare those responses on day 30 with observations from the assessment of Midwestern streams. Specifically, the direct (mortality) and indirect (altered ecological processes) effects of bifenthrin on benthic communities (larval insects and periphyton communities) and on adult aquatic insects were assessed in a manipulative experiment and extrapolated to a field survey of streams to improve causal linkages in the field study conclusions.

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MATERIALS AND METHODS Manipulative Experiment. Mesocosm Laboratory Operation. In 2014, a 30 day mesocosm test was conducted at the U.S. Geological Survey (USGS) Fort Collins Science Center. Operations of the mesocosm laboratory are detailed in SI Section 1, Figure S1. Briefly, trays filled with large gravel were colonized by macroinvertebrates in the Cache La Poudre River (Poudre River; Larimer County, Colorado). After 75 days, the trays were transported to the laboratory and placed in stream mesocosms. The mesocosms were 18.9 L buckets containing B



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were normalized by OC content. Organic carbon was analyzed on a PerkinElmer CHNS/O analyzer (Norwalk, CT) according to a modified version of US EPA 440.0.34 Sediments were dried for 3 h at 100 °C, homogenized, exposed to concentrated hydrochloric acid fumes to remove inorganic carbon, and then combusted at 925 °C in silver boats. Acetanilide was used for instrument calibration for elemental carbon. Because of small sample masses (0.005 g), the DL for bifenthrin in adult insect tissues was 50 ng/g dw. After no detections in the initial treatment composites (see Invertebrate and Periphyton Collection), a composite of both families (Chironomidae and Baetidae) from the highest treatment (20 μg bifenthrin/g dw) was reanalyzed in an attempt to provide larger sample masses to improve bifenthrin DLs. Statistical Analysis. All statistical analyses were done with R software version 3.1.3 in RStudio version 0.98.110335,36 and are detailed in SI Sections 4 and 6. Concentration−response curves (4-parameter log−logistic function, exclusive of control data) were fit to the experimental data to estimate direct effects (EC50, the concentration of bifenthrin that gives half-maximal response) of bifenthrin on abundance of scrapers and sensitive EPT (Ephemeroptera−Plecoptera−Trichoptera) and Ephemeroptera (both exclusive of the tolerant mayfly Baetis tricaudatus).13,37,38 Linear regressions across the bifenthrin concentrations were fit for Ephemeroptera metrics with and without Baetis tricaudatus and for biomass of scrapers and of Baetis tricaudatus. These metrics were used in this analysis because these groups of aquatic insects are commonly cited as sensitive to contaminants.39−41 Adult insect emergence for each treatment was summarized as daily cumulative emergence and was corrected for control emergence on the given study day to depict altered emergence patterns (timing of emergence and number of individuals) in exposed mesocosms. Because emergence was dominated by chironomids (see Results), to characterize chironomid emergence in terms of larval survival, the abundance of Chironomidae larvae was also related to bifenthrin in bulk sediment as described above for linear regression. To test if exposure to bifenthrin altered the proportion of emergers relative to the number of larvae (potential emergers), the total number of emerged chironomids from each treatment was averaged and then normalized by an estimate of the potential emergers each treatment began with (average number of larvae + adults from controls). To test for a trophic cascade, we evaluated a simple network of cause−effect relationships using a path-analytic approach42 in the R package “lavaan”.43 We hypothesized that bifenthrin in sediment would reduce the biomass of scrapers, causing an increase in the biomass of primary producers such as chlorophyll-a. Bifenthrin concentration was the exogenous (predictor) variable and scraper biomass and chlorophyll-a were endogenous (response) variables. We hypothesized that bifenthrin would not affect chlorophyll-a directly and that the effect would be fully mediated by scrapers.42 The manipulative experiment (mesocosms) and observational stream survey (MSQA) results were compared by examining graphs of bifenthrin in sediment versus percent abundance of sensitive Ephemeroptera and of scrapers for the two data sets. Risks to Midwestern streams were estimated by calculating toxicity units (TU; sensu Liess et al.44) for each site (Table S7) with detectable bifenthrin as the measured OCnormalized bifenthrin concentration divided by the mesocosmderived EC50 for scraper abundance (233.5 ng/g OC; see

for bifenthrin at the USGS Organic Chemistry Research Laboratory (OCRL; Sacramento, CA; SI Section 3). On day 30, periphyton was collected by scraping a 3 cm2 area on a rock from each mesocosm (SI Section 4). Larval invertebrates were collected by dislodging them from substrates and sieving to 500 μm. Preserved invertebrates were identified to genus or species, except for Oligochaeta, which were identified to family.29 Invertebrates were assigned to functional feeding groups, where facultative roles were ignored.29 The length of each invertebrate was measured to the nearest 1 mm, and biomasses of scrapers and Baetis tricaudatis were estimated from length-mass regressions and corrected for the area of the colonization trays.30 Bulk Sediment Collection. On day 30, bulk sediment ( 1) to depict field observations as proportions of the mesocosm-derived EC50.

compromising the entire mesocosm, so the time-weighted average concentration in the sediments across the 30 day exposure could not be calculated. Bifenthrin dissipated from the water column quickly, is hydrophobic (log Kow ∼ 6), and has a long half-life;6 we therefore hypothesize that the final (day 30) bulk sediment concentrations likely were similar to initial bulk sediment concentrations and reflect exposure concentrations when the onset of effects on macroinvertebrates occurred (likely before day 30). The mesocosm data therefore were analyzed with the final, measured bulk sediment concentrations normalized to OC. Control mesocosms were assigned a bifenthrin concentration of one-half the DL normalized to the average percentage of OC (5.1%). Average concentrations of bifenthrin in bulk sediment ranged from 2.3 to 33.8 ng/g dw and from 57.7 to 531.7 ng/g OC (Table S6). As determined in a pilot study (unpublished data),

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RESULTS Manipulative Experiment (Mesocosm) Chemistry. Bifenthrin quickly dissipated from the water column; within 10 min of spike delivery, less than 5% (range: 1.4−4.8%) of the mass of bifenthrin in the spikes remained detectable in the whole water (Table S3). At 24 h after spike delivery, the mass of bifenthrin in water (whole-water sample) was less than 1% of the mass in the spike (Table S3). Measured sediment-spike concentrations ranged from 599 to 17 313 ng/g dw (Table S5) and were 57−96% of nominal concentrations. We could not measure initial bulk sediment bifenthrin concentrations without D



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a small amount (0.5−1.2%) of the bifenthrin adsorbed to the mesocosm walls (SI Section 2, Table S1). Average water temperature in this test (13.8 ± 0.3 °C) was lower than in standard toxicity tests, but within the range of temperatures measured in the MSQA (average minimum: 14.2 °C). Effects on Larval and Adult Communities (Manipulative Experiment). Total richness ranged from 9 operational taxonomic units (OTU) at a bifenthrin concentration of 561 ng/g OC to 27 OTU in a control. Only 3 Ephemeroptera genera and a mean of 6 EPT genera were present in each replicate exposed to the highest bifenthrin concentration, whereas a mean of 9 and 16, respectively, were present in the controls. As bifenthrin concentration increased, there was a significant decrease in richness of EPT (p < 0.001, R2 = 0.43; Figure S5A) and abundance of all EPT and sensitive EPT (both p < 0.01, R2 = 0.39 and 0.57, respectively; Figure S5B). The EC50 for sensitive EPT was 197.6 ng/g OC (Figure 1A). The abundance of sensitive Ephemeroptera (Figure S5C) significantly decreased as bifenthrin concentrations increased (p < 0.01, R2 = 0.48); the EC50 was 227.2 ng/g OC (Figure 1B). Similarly, abundance and biomass of macroinvertebrates in the scraper functional feeding group significantly decreased as bifenthrin concentrations increased (both p < 0.01, R2 = 0.41 and 0.39, respectively; Figure S5D); the EC50 was 233.5 ng/g OC (Figure 1C). Chironomidae larvae abundance was not related (p = 0.10) to bifenthrin concentration (SI Section 8, Figure S6). While most larval taxa decreased in abundance across the bifenthrin concentrations, one abundant taxon, Baetis tricaudatus, increased in biomass across the bifenthrin concentrations (p < 0.001, R2 = 0.48). Additionally, the effect of bifenthrin on abundance of the order Ephemeroptera was significant only if Baetis tricaudatus was excluded (R2 = 0.44, p < 0.001) (Figure S5C,D, SI Section 7). In the manipulative experiment, emergence began on day 16 and was composed of Chironomidae (91%), Baetis sp. (8.7%), and Simulium sp. (0.2%). Emergence was stimulated (relative to the controls) when communities were exposed to the two lowest concentrations of bifenthrin (57.7 and 102.2 ng/g OC), but all other concentrations of bifenthrin suppressed cumulative emergence (relative to controls) by day 30 (Figure 2A,B). For each treatment, ratios of emergent male to female chironomids ranged from 0.9 to 1.8 males per female, and sex ratios did not vary among the treatments (p = 0.33). All Baetis sp. adults (n = 36) were males. The proportion of total emergers (relative to the average total number of larvae + adults in controls) decreased as bifenthrin concentrations increased (Figure 2B, p = 0.03, R2 = 0.73). No bifenthrin was detected in the emergent Chironomidae or Baetidae samples (n = 14) nor in the composite of both families from the highest bifenthrin treatment at a DL of 50 ng/g dw. Trophic Cascade (Manipulated Experiment). Increasing bifenthrin concentration caused a direct negative effect on scraper biomass (standardized path coefficient −0.63, R2 = 0.39; Figure 3). Controlling for this negative effect of bifenthrin on scrapers, scraper biomass also negatively affected chlorophyll-a biomass (standardized path coefficient −0.53, R2 = 0.28; Figure 3). The result of these two negative path coefficients was a net increase in chlorophyll-a as bifenthrin concentrations increased, and as a result, chlorophyll-a was significantly higher (ANOVA, F = 13.35, df = (6, 38), p = 0.002) on day 30 than at time zero in the mesocosms exposed to the highest bifenthrin concentration (SI Section 4, Figure S3). When individual mesocosm bifenthrin concentrations (as

Figure 3. Structural equation (path) model for effects of bifenthrin on scraper biomass and chlorophyll-a (ChlA) concentrations. For path coefficients, upper numbers are unstandardized coefficients and lower are standardized. dw = dry weight, OC = organic carbon.

opposed to average treatment concentrations) were considered, chlorophyll-a on day 30 was above the average control level at bifenthrin concentrations ≥314 ng/g OC. This fully mediated path model (χ2 = 2.612, p = 0.106, CFI = 0.909, SRMR = 0.090, modification index = 2.462) states that an increase of 100 ng bifenthrin/g OC was associated with a 743 mg/m2 decrease in scraper biomass and a 0.21 mg/m2 increase in chlorophyll-a (Figure 3). The direct effect between bifenthrin concentrations and chlorophyll-a biomass was not significant (modification index = 2.46, p = 0.096). Environmental Relevance of the Manipulative Experiment. Decreases in percent abundance of sensitive Ephemeroptera and of scrapers relative to total abundance were consistent between the manipulative experiment and the observational field survey (Figure 4A,B). The manipulative experiment data overlapped with the observational MSQA stream data in terms of range of bifenthrin concentrations and percent abundance of sensitive Ephemeroptera and scrapers at a given concentration. Thirty of the field sites had bifenthrin concentrations within the range of concentrations where altered emergence and periphyton biomass was observed in the mesocosm experiment (gray boxes in Figure 4A,B). Six of the field sites (7% of sites sampled) had bifenthrin concentrations that exceeded 314 ng/g OC, the concentration at and above which increased periphyton abundance was observed in the mesocosms (Figure 4A,B). For the observational study (MSQA), TUs were calculated as the OC-normalized bifenthrin concentration divided by the EC50 for scraper abundance determined from the mesocosm experiment (233.5 ng/g OC) (SI Section 5, Table S7). About 11% of the 92 field sites were classified as toxic (TU > 1, Figure 4C). An additional 10% of sites were classified as impaired (0.5 < TU ≤ 1), and 17% of sites were classified as potentially affected (0.25 < TU ≤ 0.5) by bifenthrin contamination (Figure 4C).

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DISCUSSION A novel combination of lab and field observations together support the idea that bifenthrin at concentrations previously thought safe cause both structural and functional changes to aquatic communities. Invertebrate communities in streams respond to a myriad of stressors. The experimental design offered by mesocosms allows control over other limiting factors, and the results of this study indicate that, if similar patterns between bifenthrin concentrations and ecological effects are observed in an ecosystem, those effects are likely the result of bifenthrin contamination. A single bifenthrincontaminated suspended-sediment spike delivered to mesoE



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Figure 4. Percentages of sensitive Ephemeroptera (A) and scrapers (B), corrected for total larval macroinvertebrate abundance in the sample from the mescosms and the Midwest Stream Quality Asssessment (MSQA) streams. Streams in the MSQA with no detectable bifenthrin were included in the regressions. Sensitive Ephemeroptera excluded pollution-tolerant Baetis sp. The gray box in A and B indicates the range of bifenthrin concentrations in the experimental streams where altered food web dynamics, including stimulated and suppressed emergence and loss of top down control on periphyton, began. These food web effects magnified as bifenthrin concentrations increased (to the right of the box) in the mesocosms. Additionally, the abundance of scrapers (C) is plotted against calculated bifenthrin toxicity units for 44 MSQA streams with detectable bifenthrin in the bed sediment. The red line in C denotes a toxicity unit of one, where sites to the right of this line are expected to have sediments toxic to macroinvertebrates. Toxicity units were calculated with the bifenthrin EC50 for scraper abundance (233.5 ng/g OC) from the experimental stream data. OC = organic carbon.

species with different tolerances to contaminants.25 Natural insect communities are composed of populations of organisms of mixed life stages (e.g., both immature and mature larvae) and with different susceptibilities to toxicants.45,46 In our manipulative stream mesocosm study, sensitive taxa such as Capnia sp.47 were lost from the highest treatment, while one abundant taxon, Baetis tricaudatus, significantly increased in abundance and biomass across the range in bifenthrin concentrations (Figure S5). Baetis tricaudatus has been described to have moderately high tolerance to pollutants in general37 and specifically to pyrethroids38 and has been found in high abundances in urban streams contaminated with bifenthrin.13 An increase in Baetis tricaudatus with higher bifenthrin concentrations, however, was not predicted and suggests that an advantage was conveyed to this species (SI Section 7). Bifenthrin caused a fully mediated42 trophic cascade in the mesocosms. Decreases in the number of grazing mayflies released periphyton from grazing pressure, causing a net increase in chlorophyll-a. Although this positive effect on periphyton has been observed in lentic ecosystems exposed to bifenthrin,48 trophic cascades and other indirect effects that alter food webs caused by pesticide exposure are rarely reported for lotic systems.26,48 In fact, in riverine systems, investigations of pesticide effects on carbon processing has largely been limited to effects on microbial decomposition of leaf litter or direct effects on taxa of particular feeding traits like shredders.49−51 The effects observed in our mesocosm study have implications for the management of stream algal blooms; these usually are assumed to be the result of nutrient addition but in fact might be the indirect ecosystem response to insecticides in runoff. The trophic cascade also suggests that scrapers as a group are particularly vulnerable to pyrethroids, and that algae, their primary food source, is a likely exposure route. Several other studies support these ideas. Recently, it was reported that a high surface area/weight ratio and a preference for course substrate are traits common in taxa that are particularly sensitive to

cosms resulted in exposure lasting throughout the experiment (30 days) and caused a number of ecological effects including taxa loss, a trophic cascade, and altered adult emergence. These ecological effects (results from mesocosms) occurred at a range of concentrations that were observed in numerous streams in the Midwest. Concordance between bifenthrin concentrations and taxa loss measured in the manipulative mesocosm study and the observational MSQA survey indicate that bifenthrin might be a driver of invertebrate communities in the Midwest. The intent of the manipulative mesocosm study was to simulate a single runoff event whereby bifenthrin bound to suspended sediment is transported to receiving streams. Such events expose aquatic ecosystems to a rapid pulse of aqueous bifenthrin followed by a more protracted or even chronic exposure via bulk sediments. While our aim was not to quantify the fate and transport mechanisms of such events, we did want to simulate a realistic exposure scenario for stream ecosystems. It is difficult to capture runoff events and document short-term pulse aqueous exposures to hydrophobic insecticides in real streams, thus observational studies commonly characterize concentrations of contaminants in water and sediment and relate those concentrations to metrics of ecological integrity. Our mesocosm study documented that a single suspendedsediment pulse can elicit an aqueous exposure to bifenthrin lasting less than 1 day to as long as 16 days, while bulk sediments can have elevated bifenthrin concentrations that persist for at least 30 days. Effect estimates derived from the mesocosm experiment can be considered to represent a realistic field-exposure scenario, which is different from the scenario commonly employed in sediment-toxicity bioassays. Bifenthrin contamination led to less abundant and less diverse macroinvertebrate communities, and these community effects occurred at bifenthrin concentrations substantially lower (as low as 197.6 ng/g OC) than the most commonly cited 10 day LC50 for Hyalella azteca, 520 ng/g OC.14 Mesocosms can produce more sensitive responses than a single-species toxicity test because mesocosms contain communities of interacting F



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pyrethroids.19 Experimental dosing of a forested stream with permethrin resulted in permethrin concentrations in algae 100 times the maximum water concentration, and the permethrin was reported to be more persistent in the algae than in water.52 Finally, aquatic insects cannot detect pyrethroids in food and thus do not avoid pyrethroid-contaminated food.53 Thus, pyrethroids may be trophicly available to aquatic insects and cause toxicity via dietary uptake and not just through direct contact. Only recently has aquatic adult emergence been recognized as an ecologically important end point that links aquatic and terrestrial food webs54−56 and that emergence can be altered by aquatic contaminants.57,58 We investigated the degree to which sediment-bound bifenthrin could alter the production and timing of prey items derived from aquatic ecosystems. At lower concentrations of bifenthrin, insects developed to the minimum size to complete metamorphosis17 more quickly and more frequently than that observed in controls. We hypothesize that this stimulated emergence of collector−gatherers (i.e., chironomids and baetid mayflies) was not driven by food limitations59,60 because insects do not avoid pyrethroidcontaminated food.53 Bifenthrin exposure can disrupt multiple physiological functions, eliciting altered, nonmonotonic emergence patterns. Bifenthrin is a chiral compound in which 1-Rcis-bifenthrin is more readily accumulated and toxic and 1-S-cisbifenthrin can act as an environmental estrogen.61−63 One hypothesis, therefore, is that at low bifenthrin concentrations in the mesocosms there was not sufficient 1-R-cis-bifenthrin for toxicity but that 1-S-cis-bifenthrin acted as an endocrine disruptor that stimulated emergence, producing the observed hormesis. Alternatively, because bifenthrin is a neurotoxin, at low concentrations, it might alter neurological controls on hormones that control emergence, but at higher concentrations, it might have direct toxicity resulting in delayed growth and development64 and/or lethality to larvae, processes that would slow and decrease emergence relative to controls. These altered emergence patterns (i.e., stimulation, suppression, and altered timing relative to controls) are consistent with trends observed for exposure to the pyrethroid esfenvalerate65,66 and other pesticides.59,60 The consequences of altered emergence dynamics affect both aquatic and terrestrial ecosystems. Changes in the synchrony of emergence and abundance of emergers could decrease the number of individuals that return to the aquatic ecosystem and contribute eggs to sustain future generations17,67 and/or become prey for fish.68 Second, because adult aquatic insects are prey to riparian consumers, changes in the number of aquatically derived prey items cause reciprocal responses in the number, biomass, and growth rate of riparian consumers.54,55,57 Such terrestrial ecosystem responses can be larger than those observed in the aquatic insect communities. For example, Sabo and Power54 showed that a 60% reduction in emergent aquatic insects caused a 7-fold decrease in lizard growth rates. Thus, the effects of contaminants in aquatic ecosystems can propagate to terrestrial ecosystems, and the response is not necessarily proportionate. Further, once adult aquatic insects are consumed, the aquatically derived contaminants in their bodies can accumulate in terrestrial food chains.58,69 Although bifenthrin has been detected in aquatic organisms,70,71 we did not detect it in adults emerging from the mesocosms; however, our DL was large because of small sample mass. In light of frequently cited differences between mesocosms and real-world ecosystems,20 we compared the results of the

mesocosm study to those of the regional stream assessment with the intent of using mesocosm-derived bifenthrin effect estimates to scale risks to aquatic life observed in Midwestern streams. Such an evaluation provides better causal linkages between effects benchmarks and observed effects because the benchmarks were developed under controlled, single-stressor conditions whereas field communities are responding to multiple stressors. Also, mesocosm tests offer the ability to measure important (as observed here) multitaxon indirect effects, which cannot be observed in single species bioassays. The high variability in the Midwest Stream Quality Assessment (MSQA) data, especially at low bifenthrin concentrations, is expected for a field assessment, and the lack of a strong relation between bifenthrin and abundance metrics at low concentrations indicates that other factors (e.g., habitat, flow, other contaminants) are limiting macroinvertebrate abundances at these sites.72 Despite this variability, the mesocosm and MSQA data were concordant for two selected abundance metrics, as indicated by the overlap of the two data sets (Figure 4). This overlap and shape of the data suggests that, at least in part, the MSQA communities were limited (sensu Schmidt et al.72) by bifenthrin in sediment, especially at higher concentrations where TU exceeded 1. Furthermore, on the basis of estimates from our mesocosm experiment, 17% of 92 streams studied in the Midwest had a TU greater than 0.5, indicating likely impairment of aquatic insect communities caused by exposure to bifenthrin, and about 40% of streams are expected to have altered aquatic and/or aquatic-terrestrial food web dynamics. As pyrethroid, and specifically bifenthrin, use continues to increase,4 we expect food web dynamics in more streams in the Midwest and in other regions of the United States and worldwide that are undergoing agricultural intensification to become impaired and regional aquatic biodiversity to further decrease.3 Given the low water temperature of the mesocosm experiment compared to standard toxicity-test temperature (usually 25 °C), the mesocosm test was more realistic of exposure scenarios in natural streams with cool water temperatures,73−75 such as the MSQA streams (average minimum of 14.2 °C and average of 20.8 °C during the summertime sampling). The inverse relation between temperature and pyrethroid toxicity10,76 suggests that biota in these streams could experience the greatest toxic effects during colder periods of the day or even the year, if bifenthrin applied in summer is still adsorbed to the sediments in winter, which is possible with its long half-life.6 The lower temperature of the mesocosms relative to standard toxicity tests is a possible explanation for the higher sensitivity of the mesocosm community metrics. The mesocosm study provides insight into ecological processes and mechanisms by which bifenthrin, and potentially other pyrethroids, alter aquatic and terrestrial ecosystems. Effects ranged from direct mortality of benthic macroinvertebrates to disruption of stream community balance, and such adverse effects are likely extensive in the Midwest where bifenthrin contamination is widespread. Effects of bifenthrin contamination propagate across life stages and generations of invertebrates, trophic levels in aquatic food webs, and ecosystem boundaries to riparian food webs, and bifenthrin contamination therefore has the potential to affect terrestrial as well as aquatic communities. Previous reports that pesticides are shaping global freshwater biodiversity have focused on taxa loss. Our study suggests that, in areas where biodiversity is G



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(2) Stehle, S.; Schulz, R. Agricultural insecticides threaten surface waters at the global scale. Proc. Natl. Acad. Sci. U. S. A. 2015, 112 (18), 5750−5755. (3) Beketov, M. A.; Kefford, B. J.; Schafer, R. B.; Liess, M. Pesticides reduce regional biodiversity of stream invertebrates. Proc. Natl. Acad. Sci. U. S. A. 2013, 110 (27), 11039−43. (4) National Water-Quality Assessment Program Pesticide Use Maps - Bifenthrin. https://water.usgs.gov/nawqa/pnsp/usage/maps/show_ map.php?year=2013&map=BIFENTHRIN&hilo=L (Accessed Jan 8, 2016). (5) Transparency Market Research. Bifenthrin Market - Global Industry Analysis, Size, Share, Trends, Forecast, 2014−2020. http:// www.transparencymarketresearch.com/bifenthrin-market.html. (6) Gan, J.; Lee, S. J.; Liu, W. P.; Haver, D. L.; Kabashima, J. N. Distribution and persistence of pyrethroids in runoff sediments. J. Environ. Qual. 2005, 34, 836−841. (7) Hladik, M. L.; Kuivila, K. M. Pyrethroid insecticides in bed sediments from urban and agricultural streams across the United States. J. Environ. Monit. 2012, 14 (7), 1838−1845. (8) Budd, R.; Bondarenko, S.; Haver, D.; Kabashima, J.; Gan, J. Occurrence and bioavailability of pyrethroids in a mixed land use watershed. J. Environ. Qual. 2007, 36, 1006−1012. (9) Weston, D. P.; Poynton, H. C.; Wellborn, G. A.; Lydy, M. J.; Blalock, B. J.; Sepulveda, M. S.; Colbourne, J. K. Multiple origins of pyrethroid insecticide resistance across the species complex of a nontarget aquatic crustacean, Hyalella azteca. Proc. Natl. Acad. Sci. U. S. A. 2013, 110 (41), 16532−16537. (10) Weston, D. P.; You, J.; Harwood, A. D.; Lydy, M. J. Whole sediment toxicity identification evaluation tools for pyrethroid insecticides: III. Temperature manipulation. Environ. Toxicol. Chem. 2009, 28 (1), 173−180. (11) Delgado-Moreno, L.; Lin, K.; Veiga-Nascimento, R.; Gan, J. Occurrence and toxicity of three classes of insecticides in water and sediment in two southern California coastal watersheds. J. Agric. Food Chem. 2011, 59, 9448−9456. (12) Hall, L. W., Jr.; Anderson, R. D. Relationship between bifenthrin sediment toxic units and benthic community metrics in urban California streams. Arch. Environ. Contam. Toxicol. 2013, 65, 173−182. (13) Carpenter, K. D.; Kuivila, K. M.; Hladik, M. L.; Haluska, T.; Cole, M. B. Storm-event-transport of urban-use pesticides to streams likely impairs invertebrate assemblages. Environ. Monit. Assess. 2016, 188 (6), 1−18. (14) Amweg, E. L.; Weston, D. P.; Ureda, N. M. Use and toxicity of pyrethroid pesticides in the Central Valley, California, USA. Environ. Toxicol. Chem. 2005, 24 (4), 966−972. (15) Harwood, A. D.; Rothert, A. K.; Lydy, M. J. Using Hexagenia in sediment bioassays: Methods, applicability, and relative sensitivity. Environ. Toxicol. Chem. 2014, 33, 868−874. (16) Benoit, D. A.; Sibley, P. K.; Juenemann, J. L.; Ankley, G. T. Chironomus tentans life-cycle test: Design and evaluation for use in assessing toxicity of contaminated sediments. Environ. Toxicol. Chem. 1997, 16 (6), 1165−1176. (17) Sibley, P. K.; Benoit, D. A.; Ankley, G. T. The significance of growth in Chironomus tentans sediment toxicity tests: Relationship to reproduction and demographic endpoints. Environ. Toxicol. Chem. 1997, 16 (2), 336−345. (18) Poteat, M. D.; Buchwalter, D. B. Four reasons why traditional metal toxicity testing with aquatic insects is irrelevant. Environ. Sci. Technol. 2014, 48 (2), 887−8. (19) Wiberg-Larsen, P.; Graeber, D.; Kristensen, E. A.; BaattrupPedersen, A.; Friberg, N.; Rasmussen, J. J. Trait characteristics determine pyrethroid sensitivity in nonstandard test species of freshwater macroinvertebrates: a reality check. Environ. Sci. Technol. 2016, 50 (10), 4971−4978. (20) Lamberti, G. A.; Steinman, A. D. Research in artifical streams: Applications, uses, and abuses. Journal of the North American Benthological Society 1993, 12 (4), 313−384, http://www.jstore.org/ stable/1467618,.

impaired by pyrethroids, ecological processes essential to aquatic and aquatic-dependent ecosystems also are very likely impaired.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.6b02761. Information describing mesocosm operations, methodology, and results for bifenthrin adsorption to mesocosm walls, analytical chemistry methods, periphyton collection methods, Midwest Stream Quality Assessment (MSQA) sampling and results, methods for determination of dry weight bifenthrin concentrations for high water content samples, statistical analysis methods, results for Baetis tricaudatus abundance and biomass path models, and emergence. Tables containing adsorbed bifenthrin concentrations; bifenthrin concentrations in the sediment, whole water, and dissolved phases in the mesocosms; estimated bifenthrin concentrations for high water content samples; bifenthrin concentrations in sediment spikes and final bulk sediments; bifenthrin concentrations and toxicity units in MSQA sediments; summary of 4-parameter logistic models. Figures containing photos of the mesocosm laboratory, a graph comparing nominal and measured bifenthrin concentrations used to estimate bifenthrin concentrations in high water content samples, graphs of periphyton chlorophyll-a biomass, a map of the MSQA sites, linear regressions of richness and abundance metrics for the mesocosm experiment, path models for Baetis tricaudatus, and a graph illustrating the relation between Chironomidae larvae and bifenthrin concentrations in the mesocosm test (PDF)

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AUTHOR INFORMATION

Corresponding Author

*Phone: 970-226-9470; fax: 970-226-9230; e-mail: tschmidt@ usgs.gov. Notes

The authors declare no competing financial interest. Data used in this publication, including a complete taxa list for the mesocosm experiment, are available on USGS ScienceBase (http://dx.doi.org/10.5066/F7SX6BBZ).

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ACKNOWLEDGMENTS This research was funded by the USGS National Water Quality Assessment Project Regional Stream Quality Assessments study and Contaminant Biology Program. We thank Janet Miller and Patricia Nease for laboratory assistance; Monique Adams, Ruth Wolf, Megan McWayne, Corey Sanders, and Matthew De Parsia for analytical assistance; Timberline Aquatics for the invertebrate identifications. Amy McMahon (USGS) assisted in the organization of the TOC/abstract art work. We thank Daren Carlisle, Brian Caruso, and three anonymous reviewers for their insightful and helpful reviews of this work. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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