Multi-region assessment of chemical mixture exposures and predicted cumulative effects in USA wadeable urban/agriculture-gradient streams

https://doi.org/10.1016/j.scitotenv.2021.145062Get rights and content

Highlights

  • Exposures to 389 organic contaminants assessed in 305 streams in 4 US regions

  • About 78% were detected with maximum cumulative concentrations >156 μg/L

  • Contaminant summary metrics correlated to watershed development metrics.

  • High probability of vertebrate molecular effects and invertebrate acute toxicity

  • Organic contaminants contribute to headwater stream multi-stressor adverse effects.

Abstract

Chemical-contaminant mixtures are widely reported in large stream reaches in urban/agriculture-developed watersheds, but mixture compositions and aggregate biological effects are less well understood in corresponding smaller headwaters, which comprise most of stream length, riparian connectivity, and spatial biodiversity. During 2014–2017, the U.S. Geological Survey (USGS) measured 389 unique organic analytes (pharmaceutical, pesticide, organic wastewater indicators) in 305 headwater streams within four contiguous United States (US) regions. Potential aquatic biological effects were evaluated for estimated maximum and median exposure conditions using multiple lines of evidence, including occurrence/concentrations of designed-bioactive pesticides and pharmaceuticals and cumulative risk screening based on vertebrate-centric ToxCast™ exposure-response data and on invertebrate and nonvascular plant aquatic life benchmarks. Mixed-contaminant exposures were ubiquitous and varied, with 78% (304) of analytes detected at least once and cumulative maximum concentrations up to more than 156,000 ng/L. Designed bioactives represented 83% of detected analytes. Contaminant summary metrics correlated strong-positive (rho (ρ): 0.569–0.719) to multiple watershed-development metrics, only weak-positive to point-source discharges (ρ: 0.225–353), and moderate- to strong-negative with multiple instream invertebrate metrics (ρ: −0.373 to −0.652). Risk screening indicated common exposures with high probability of vertebrate-centric molecular effects and of acute toxicity to invertebrates, respectively. The results confirm exposures to broad and diverse contaminant mixtures and provide convincing multiple lines of evidence that chemical contaminants contribute substantially to adverse multi-stressor effects in headwater-stream communities.

Introduction

Freshwater stream ecosystems in urban/agriculture-developed watersheds reflect aggregated impacts of multiple instream physical, chemical, and biological alterations (stressors) derived from multiple lateral (landscape) and longitudinal (upstream) sources (e.g., Birk et al., 2020; Nilsen et al., 2019; Posthuma et al., 2016, Posthuma et al., 2018; Waite et al., 2019). Consequently, instream ecological structure and function indices frequently correlate well with broad landscape-scale predictors, like watershed-development metrics, while the effects contributions of individual or subclasses of stressors, which are typically the more-tractable target scales for mitigation and management, are frequently difficult to deconvolve and assess (Berger et al., 2016; Bradley et al., 2019; Posthuma et al., 2016; Schäfer et al., 2016; Waite et al., 2019). Limited data on possible adverse biological effects of contaminant mixtures in developed headwater streams are recognized challenges to management of multi-stressor impacts in freshwater fluvial networks (e.g., Alexander et al., 2007; Bishop et al., 2008; Bradley et al., 2019; Lowe and Likens, 2005; Paulsen et al., 2006).

Historical focus on higher-order stream reaches, where dilution-dependent, point sources like wastewater treatment facility (WWTF) discharges are preferentially located (e.g., Bradley et al., 2019; Luo et al., 2014; Michael et al., 2013; Monteiro and Boxall, 2010) and extensive organic-contaminant cocktails are widely reported (Brack et al., 2015; Bradley et al., 2017; Le et al., 2017; Malaj et al., 2014; Rosi-Marshall and Royer, 2012), contrasts with comparatively limited water-quality assessments in spatially and temporally variable headwater reaches. Headwater streams are fluvial capillaries (Lowe and Likens, 2005) that dominate total stream length (Downing et al., 2012; Leopold, 1962) and landscape-scale hydrologic connectivity (Bishop et al., 2008; Downing et al., 2012; Freeman et al., 2007; Leopold, 1962) and provide critical habitat variability (Downing et al., 2012; Freeman et al., 2007) and biodiversity (Biggs et al., 2017; Clarke et al., 2008; Lowe and Likens, 2005; Meyer et al., 2007). Thus, improved understandings of contaminant-mixture compositions, variability, and aggregated effects in developed-watershed headwater streams are priorities (Alexander et al., 2007; Cappiella et al., 2012; McKinney, 2006; Scheffers and Paszkowski, 2012), in the face of increasing global urbanization (United Nations, 2014) and concomitant built-environment habitat fragmentation (Grimm et al., 2008; Tu, 2011).

The 2013–2017 U.S. Geological Survey (USGS) Regional Stream Quality Assessments (RSQA) were initiated to further inform the impacts of multiple stressors, including mixed organic contaminants, on instream ecological structure and function in the wadeable headwaters of the contiguous United States (US). Five broad regions distributed across the contiguous US were selected for study in sequential years to realize resource-intensive spatial and single-season temporal regional assessments that together informed a national-scale perspective of potential multi-stressor drivers of headwater-stream ecosystem health. After the initial 2013 agriculture-gradient Midwest (MSQA) (Garrett et al., 2017) study and its corresponding focus on pesticides (Mahler et al., 2017; Nowell et al., 2018; Van Metre et al., 2017), the RSQA organic-contaminant toolbox was expanded to include organic indicators of domestic and industrial wastewater to better reflect the mixed urban/agriculture-gradient study areas in the Southeast (SESQA, 2014 (Journey et al., 2015)), the Pacific Northwest (PNSQA, 2015 (Sheibley et al., 2017)), the Northeast (NESQA, 2016 (Coles et al., 2019)), and coastal California (CSQA, 2017 (May et al., 2020)). For SESQA, results of surface-water samples, collected at varying times over a 10-week water-quality index period and analyzed using 5 target-organic methods (pesticides, pharmaceuticals, organic wastewater indicators [OWI], and 2 volatile organic compounds [VOC]; 475 unique organic analytes), were aggregated to estimate maximum and median aquatic-exposure conditions and explore a multiple lines of evidence approach to assessing mixture effects (Bradley et al., 2019). Based on the SESQA findings, subsequent studies (PNSQA, NESQA, CSQA) retained an analytical toolbox focused on pesticides, pharmaceuticals, and organic wastewater indicators (OWI) (389 unique analytes) as metrics to support inter-region comparisons of urban/agriculture-development organic-contaminant impacts. An earlier report was focused only on inter-regional comparisons of instream exposures and sublethal effects of pharmaceutical contaminants generally attributed to wastewater sources (Bradley et al., 2020a).

Herein results for all three organic contaminant methods were aggregated to estimate acute (maximum) and chronic (median) cumulative-exposure conditions for the 305 wadeable headwater streams assessed across the four regions (including SESQA) during 2014–17. Potential predictors of instream mixed-contaminant exposure were assessed based on correlations with individual contaminants and with readily available geographic information system (GIS) land-use land-cover (LULC) metrics. A simplified multiple lines of evidence approach (Bradley et al., 2019) was employed to assess the potential organic-contaminant risk (Moretto et al., 2017; National Research Council, 1983; Norton et al., 1992; Rodier and Norton, 1992) to instream biota, including: 1) occurrence and cumulative concentrations of pesticide and pharmaceutical compounds designed to be biologically active (hereafter referred to as designed-bioactives) (Bradley et al., 2019), 2) cumulative contaminant risk indices (Goumenou and Tsatsakis, 2019; U.S. Environmental Protection Agency, 2003, U.S. Environmental Protection Agency, 2011), including cumulative Exposure-Activity Ratio(s) (EAR) (Blackwell et al., 2017) based on exposure-response relations in ToxCast™ (U.S. Environmental Protection Agency, 2020b) and cumulative Toxicity Quotients (∑TQ) (Corsi et al., 2019) based on US Environmental Protection Agency (EPA) Office of Pesticide Programs (OPP) Aquatic Life (AL) acute benchmarks for invertebrates and nonvascular plants (U.S. Environmental Protection Agency, 2020d), and 3) Spearman Rank correlations of instream ecological metrics with cumulative and individual contaminant metrics.

Section snippets

Site description and sample collection

Water samples were collected by USGS from perennial, wadeable (less than 10 m width and 1 m depth at base flow) headwater stream sites in watersheds with varying degrees of urban and agricultural land use as part of four regional assessments during 2014–2017 (Figs. 1, S1; Table S1). Site selection and sampling methodologies are described in detail elsewhere (Coles et al., 2019; Journey et al., 2015; May et al., 2020; Sheibley et al., 2017). During each water-quality assessment period

Mixed-contaminant exposures and predictors

Among the 305 wadeable streams sampled for all three methods across all 2014–2017 RSQA study regions, mixtures (≥2 detected analytes) of organic contaminants were predicted under the estimated maximum exposure conditions in all 261 multiple-sample, urban/agriculture-gradient sites and in all but 2 (95%) of the 44 single-sample, undeveloped, presumptive low-impact, sites (Fig. 1, Fig. 2, Tables S3–S4). Crucially, contaminant mixtures were detected under the estimated median exposure conditions

Conclusions

The risk of mixed-organic contamination to aquatic organisms in urban/agriculture-gradient headwater streams in four US regions was assessed based on 1) observed instream exposures to an indicator suite of 395 target analytes and 2) multiple lines of evidence for biological effects. Extensive and diverse contaminant mixtures were pervasive in RSQA study streams across the US. Instream contaminant exposures were more strongly correlated with broad landscape-scale development metrics than with

CRediT authorship contribution statement

Paul M. Bradley: Conceptualization, Methodology, Formal analysis, Investigation, Writing – original draft, Writing – review & editing, Visualization. Celeste A. Journey: Formal analysis, Investigation, Data curation, Writing – review & editing. Kristin M. Romanok: Formal analysis, Data curation, Writing – review & editing. Sara E. Breitmeyer: Formal analysis. Daniel T. Button: Data curation. Daren M. Carlisle: Investigation. Bradley J. Huffman: Formal analysis. Barbara J. Mahler: Investigation.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This research was conducted and funded by the USGS National Water Quality Program's Regional Stream Quality Assessment. Additional support for Bradley, Breitmeyer, Huffman, Romanok, and Smalling was provided by the USGS Environmental Health Programs. We thank Karen Beaulieu of the USGS and 3 anonymous journal referees for their reviews. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government.

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