Contaminants of emerging concern in tributaries to the Laurentian Great Lakes: II. Biological consequences of exposure

<div><p>The Laurentian Great Lakes contain one fifth of the world’s surface freshwater and have been impacted by human activity since the Industrial Revolution. In addition to legacy contaminants, nitrification and invasive species, this aquatic ecosystem is also the recipient of Contaminants of Emerging Concern (CECs) with poorly understood biological consequences. In the current study, we documented the presence, concentrations, and biological effects of CECs across 27 field sites in six Great Lakes tributaries by examining over 2250 resident and caged sunfish (<i>Lepomis ssp</i>.) for a variety of morphological and physiological endpoints and related these results to CEC occurrence. CEC were ubiquitous across studies sites and their presence and concentrations in water and sediment were highest in effluent dominated rivers and downstream of municipal wastewater treatment plant discharges. However, even putative upstream reference sites were not free of CEC presence and fish at these sites exhibited biological effects consistent with CEC exposure. Only the Fox River exhibited consistent adverse biological effects, including increased relative liver size, greater prominence of hepatocyte vacuoles and increased plasma glucose concentrations. Canonical Redundancy Analysis revealed consistent patterns of biological consequences of CEC exposure across all six tributaries. Increasing plasma glucose concentrations, likely as a result of pollutant-induced metabolic stress, were associated with increased relative liver size and greater prominence of hepatocyte vacuoles. These indicators of pollutant exposure were inversely correlated with indicators of reproductive potential including smaller gonad size and less mature gametes. The current study highlights the need for greater integration of chemical and biological studies and suggests that CECs in the Laurentian Great Lakes Basin may adversely affect the reproductive potential of exposed fish populations.</p></div

Contaminants of emerging concern in tributaries to the Laurentian Great Lakes: I. Patterns of occurrence

<div><p>Human activities introduce a variety of chemicals to the Laurentian Great Lakes including pesticides, pharmaceuticals, flame retardants, plasticizers, and solvents (collectively referred to as contaminants of emerging concern or CECs) potentially threatening the vitality of these valuable ecosystems. We conducted a basin-wide study to identify the presence of CECs and other chemicals of interest in 12 U.S. tributaries to the Laurentian Great Lakes during 2013 and 2014. A total of 292 surface-water and 80 sediment samples were collected and analyzed for approximately 200 chemicals. A total of 32 and 28 chemicals were detected in at least 30% of water and sediment samples, respectively. Concentrations ranged from 0.0284 (indole) to 72.2 (cholesterol) μg/L in water and 1.75 (diphenhydramine) to 20,800 μg/kg (fluoranthene) in sediment. Cluster analyses revealed chemicals that frequently co-occurred such as pharmaceuticals and flame retardants at sites receiving similar inputs such as wastewater treatment plant effluent. Comparison of environmental concentrations to water and sediment-quality benchmarks revealed that polycyclic aromatic hydrocarbon concentrations often exceeded benchmarks in both water and sediment. Additionally, bis(2-ethylhexyl) phthalate and dichlorvos concentrations exceeded water-quality benchmarks in several rivers. Results from this study can be used to understand organism exposure, prioritize river basins for future management efforts, and guide detailed assessments of factors influencing transport and fate of CECs in the Great Lakes Basin.</p></div

Heatmap of two-way cluster analysis performed on rank-transformed sediment data (only includes chemicals detected ≥30% of sediment samples).

<p>Data ranks are represented by color; lighter colors correspond to lower ranks. E2, 17β-estradiol; OP, 4-<i>tert</i>-octylphenol; ANQN, anthraquinone; BSS, β-sitosterol; BSM, β-stigmastanol; CHOL, cholesterol; IND, indole; MIND, 3-methyl-indole; MP, <i>p</i>-cresol; ISO, isophorone; DPHD; diphenhydramine; DCBZ, 1,4-dichlorobenzene; AHTN, acetyl hexamethyl tetrahydronaphthalene; HHCB, hexahydrohexamethyl cyclopentabenzopyran; A4, 4-androsterne-3,17-dione; AND, <i>cis</i>-androsterone; DMNAP, 2,6-dimethylnaphthalane; E1, estrone; BPA, bisphenol A; NAP, naphthalene; 1-MNAP, 1-methylnaphthalene; 2-MNAP, 2-methylnaphthalene; CARB, carbazole; ANT, anthracene; BaP, benzo(a)pyrene; PHEN, phenanthrene; FLU, fluoranthene; PYR, pyrene.</p

Canonical redundancy analysis for water samples and biological results.

<p>(A) Resident females, (B) Resident males, (C) Caged females, and (D) Caged males. Number in parentheses on axes indicate the percent variability that is explained by that axis. Sample site information can be found in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0184725#pone.0184725.t001" target="_blank">Table 1</a>. Sample class information can be found in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0184725#pone.0184725.t002" target="_blank">Table 2</a>. Biological response information can be found in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0184725#pone.0184725.t004" target="_blank">Table 4</a>, Figs <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0184725#pone.0184725.g002" target="_blank">2</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0184725#pone.0184725.g005" target="_blank">5</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0184725#pone.0184725.s006" target="_blank">S6</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0184725#pone.0184725.s009" target="_blank">S9</a> Figs, and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0184725#pone.0184725.s015" target="_blank">S3 Table</a>.</p

Biological endpoints in resident male sunfish.

<p>(A) hepatosomatic index; (B) prevalence of vacuoles in hepatocytes ranked on a severity scale of 1 to 4; (C) plasma vitellogenin concentration (μg/mL); and (D) plasma glucose concentration (mg/mL). Sample river location located above panels (A) and (B), with columns representing upstream to downstream within each river from left to right. Specific sample site identification can be found in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0184725#pone.0184725.t001" target="_blank">Table 1</a>. Column graphs indicate mean + standard deviation in panels (A) and (B). Box-and-whisker plots indicate range, 25^th and 75^th percentiles, and mean values in panels (C) and (D). Statistical significance (Kruskal-Wallis with Dunn’s post-test; p<0.05) within panels are identified by letters. P-values are summarized in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0184725#pone.0184725.s016" target="_blank">S4 Table</a>. Sample size provided in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0184725#pone.0184725.s015" target="_blank">S3 Table</a>.</p

Great Lakes Basin map showing U.S. tributaries sampled in 2013–14.

<p>Numbers indicate the river basin sampled within the designated watershed. Colors depict land use as described in Homer et al. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0182868#pone.0182868.ref026" target="_blank">26</a>]. Generally, red/pink represent developed, yellow/brown represent agriculture, greens are forest, and blues are wetlands and open water.</p

CEC concentration in sediment summed by class.

<p>CEC concentration in sediment summed by class.</p

Heatmap of two-way cluster analysis performed on rank-transformations of maximum concentrations detected per site (only includes chemicals detected ≥30% of water samples).

<p>Data ranks are represented by color; lighter colors correspond to lower ranks. NIC, nicotine; ISO, isophorone; ATZ, atrazine; METCH, metolachlor; IND, indole; BSS, β-sitosterol; CHOL, cholesterol; CAFF, caffeine; DEET, N,N-Diethyl-<i>meta</i>-toluamide; COP, 3β-coprostanol; ANQN, 9,10-anthraquinone; FLU, fluoranthene; PYR, pyrene; ATEN, atenolol; COT, cotinine; FYROL FR2, tris (dichloroisopropyl) phosphate; TBEP, tris(2-butoxyethyl) phosphate; ACYC, acyclovir; METF, metformin; LID, lidocaine; HHCB, hexahydrohexamethyl cyclopentabenzopyran; METP, metoprolol; METHO, methocarbamol; MPB, meprobamate; SMX, sulfamethoxazole; MBTZ, methyl-1<i>H</i>-benzotriazole; TRIAM, triamterene; FEXO, fexofendadine; CMZ, carbamazepine; TRAM, tramadol; DESVEN, desvenlafaxine; VEN, venlafaxine.</p

Chemicals of emerging concern detected in at least 30% of all surface-water and sediment samples collected from U.S. tributaries to the Great Lakes, 2013–14.

<p>Chemicals of emerging concern detected in at least 30% of all surface-water and sediment samples collected from U.S. tributaries to the Great Lakes, 2013–14.</p