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