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Substituted Diphenylamine Antioxidants and Benzotriazole UV Stabilizers in Aquatic Organisms in the Great Lakes of North America: Terrestrial Exposure and Biodilution Zhe Lu, Amila O. De Silva, Daryl McGoldrick, Wenjia Zhou, Thomas E. Peart, Cyril J Cook, Gerald Tetreault, Pamela A. Martin, and Shane Raymond de Solla Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b05214 • Publication Date (Web): 29 Dec 2017 Downloaded from http://pubs.acs.org on December 31, 2017
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Environmental Science & Technology
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Substituted Diphenylamine Antioxidants and Benzotriazole UV Stabilizers in
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Aquatic Organisms in the Great Lakes of North America: Terrestrial Exposure and
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Biodilution
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Zhe Lu,† Amila O. De Silva,†* Daryl J. McGoldrick,† Wenjia Zhou,† Thomas E. Peart,† Cyril Cook,†
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Gerald R. Tetreault,† Pamela A. Martin,# Shane R. de Solla,#
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†
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Ontario, L7S 1A1Canada
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#
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Ontario, L7S 1A1 Canada
Water Science & Technology Directorate, Environment and Climate Change Canada, Burlington,
Ecotoxicology and Wildlife Health Division, Environment and Climate Change Canada, Burlington,
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Email addresses:
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[email protected] (Zhe Lu);
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[email protected] (Amila De Silva)
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[email protected] (Daryl McGoldrick)
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[email protected] (Wenjia Zhou)
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[email protected] (Thomas Peart)
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[email protected] (Cyril Cook)
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[email protected] (Gerald Tetreault)
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[email protected] (Pamela Martin)
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[email protected] (Shane de Solla)
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*Corresponding author: Amila O. De Silva, Tel.: 1-905-336-4407, E-mail:
[email protected]
Words: 5600(from Abstract to Acknowledgements) + 2 tables + 2 figures = 6800. 1 Environment ACS Paragon Plus
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ABSTRACT Substituted diphenylamine antioxidants (SDPAs) and benzotriazole UV stabilizers (BZT-UVs) are
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industrial
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biomagnification and spatial distribution of these contaminants in the Great Lakes of North America
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are unknown. The present study addresses these knowledge gaps by reporting SDPAs and BZT-UVs in
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herring gull (Larus argentatus) eggs, lake trout (Salvelinus namaycush) and their food web in the Great
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Lakes for the first time. Herring gull eggs showed much higher detection frequency and concentrations
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of target SDPAs and 2-(2H-benzotriazol-2-yl)-4,6-di-tert-pentylphenol(UV328) than that of the whole
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body fish homogenate. For herring gull eggs, the samples from upper Great Lakes contained
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significantly greater levels of SDPAs than those eggs from lower lakes, possibly due to the differences
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in terrestrial food in diet. Interestingly, the predominant SDPAs in herring gull eggs were dinonyl-
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(C9C9) and monononyl-diphenylamine (C9) which were previously shown to be less bioaccumulative
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than other SDPAs in fish. In contrast, dioctyl-diphenylamine(C8C8) was the major SDPA in lake trout
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and biodilution of C8C8 was observed in a Lake Superior lake trout food web. Such variations in
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herring gull eggs and fish indicate the differences in accumulation and elimination pathways of SDPAs
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and BZT-UVs and require further elucidation of these mechanisms.
additives
of
emerging
environmental
concern.
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However,
the
bioaccumulation,
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INTRODUCTION
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Substituted diphenylamine antioxidants (SDPAs) and benzotriazole UV stabilizers (BZT-UVs) are
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industrial additives applied in industrial and consumer products such as fuel, lubricant, plastics and
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rubber to minimize theoxidative degradation or UV radiation-induced color change of materials.1-
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3
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(Table S1).1,3-6Therefore, many SDPAs and BZT-UVs have been identified and managed as High
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Production Volume chemicals (e.g., as defined by Toxic Substances Control Act in the U.S.) and may
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pose risks to ecosystems and human health.5,6In Europe, some SDPAs and BZT-UVs have been
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considered as PBT (Persistent, Bioaccumulative and Toxic) chemicals and managed as Substances of
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Very High Concern (Table S1). 6
SDPAs and BZT-UVs are produced and consumed in large volumes in North America and Europe
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Many of these contaminants have been detected in environmental compartments such as
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wastewater, biosolids, surface water, sediments and biota samples, and they tend to partition to organic
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carbon and lipids.1-3The estimated log n-octanol/water partition coefficient (log Kow) of the target
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SDPAs and BZT-UVs in the present study ranged between 5.3-12.2 and 5.6-7.7, respectively;1,3given
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that many hydrophobic compounds with log Kow≥ 5 tend to biomagnify in aquatic ecosystems,7 some
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of these compounds are expected to biomagnify in food web and result in high exposure risks in top
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predators. In addition, SDPAs and BZT-UVs preferentially accumulate in the fish liver compared to
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other tissues and the biliary excretion of these contaminants is very limited in fish.8Although the
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information on their toxicity is limited, they may have chronic adverse effects on endocrine systems
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based on available mammalian and fish evaluations.9-12For example, BZT-UVs could lead to sex-
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specific chronic toxicities in rats9 and may have endocrine disruption properties in humans10 and
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fish.11,12 To date, there are no published studies on SDPA toxicity. However, U.S. EPA assessments
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reported some chronic adverse effects such as liver, blood, reproductive and developmental toxicities
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of SDPAs in rats.13-15As such, there is a strong rationale for studying the distribution, fate and toxicities
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of these contaminants in the environment for ecological risk assessment and informed management of
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these chemicals.
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Lu et al.1 recently reported the occurrence and distribution of SDPAs and BZT-UVs in water,
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sediment and biota from an urban creek in the Great Lakes region. High levels of these contaminants
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were detected in the crayfish (Orcoescties spp.) (up to 5.5 µg g-1for total (Ʃ) SDPAs and 1.3 µg g-1 for
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UV328, lipid weight (lw)).1The organisms in Great Lakes may also accumulate high levels of SDPAs
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and BZT-UVs because the Great Lakes receive water and particulate from an abundance of
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creeks/rivers affected by human activity (e.g., the effluent of wastewater treatment plant (WWTPs)).1,3
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However, the occurrence and environmental fate of these contaminants in the biota in the Great
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Lakes have never been reported. Great Lakes contain 21% of the surface freshwater on Earth and a
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human population exceeding 30 million in this region.16To protect the water resources and ecosystems
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in the Great Lakes, the updated U.S.-Canada Great Lakes Water Quality Agreement specifically
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recommends efforts on the identification and monitoring of chemicals of emerging concern in this
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region.17In the present study, the distribution of SDPAs and BZT-UVs in top predators in the Great
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Lakes was investigated, and their food web biomagnification potential.
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The adult herring gull (Larus argentatus) is an ideal avian species to track the bioaccumulation of
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organic contaminants in the Great Lakes region.18-20The herring gull is an opportunistic piscivore with
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a high breeding colony fidelity that lives year round in the Great Lakes.18-20Therefore, their eggs have
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been used as indicators of chemical contamination in the Great Lakes Herring Gull Contaminant
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Monitoring program for more than 40 years.18-20These eggs have a relatively high lipid content and
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may accumulate high levels of hydrophobic organic contaminants.19As hydrophobic compounds with
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high production volume, some SDPAs and BZT-UVs may be accumulated in herring gull eggs. Thus
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far, the occurrence of SDPAs has not been reported in any avian species, while BZT-UVs have been
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detected in the liver of wild-caught spot-billed duck (Anas poecilorhyncha) and mallard (Anas
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platyrhynchos) from Ariake Sea (Japan).21Nevertheless, no study has investigated the early-life 5 Environment ACS Paragon Plus
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exposure of bird eggs to these contaminants. Lake trout (Salvelinus namaycush) and walleye (Sander
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vitreus) are upper trophic level fish and are widely used in Fish Contaminants Monitoring and
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Surveillance Program as indicators of environmental contamination.22Lake trout are consumed on a
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regular basis by some communities in northern Canada23and are also a component of commercial and
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sport fisheries, thereby presenting a route for human exposure to contaminants. These potential
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exposure risks provide a rationale for determination of SDPAs and BZT-UVs in lake trout and
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associated food webs. Furthermore, lake trout and walleye are likely representative of other
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commercial and sport fisheries, and levels in those species provide some first information on potential
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exposure levels of humans and piscivorous wildlife.
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As the first study of SDPAs and BZT-UVs in Great Lakes organisms, we report the occurrence,
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spatial distribution and composition of these contaminants in herring gull eggs and top predator fish,
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lake trout and walleye, and evaluate the bioaccumulation of these contaminants in a food web in Lake
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Superior. Further, we used stable isotopes (δ15N, δ13C) and essential fatty acids to elucidate feeding
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ecology of the herring gulls throughout the Great Lakes, and how it affects body burdens of SDPAs and
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BZT-UVs. Our hypotheses were: (1) biota samples near emissions from larger industrial and municipal
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sources have higher levels of these contaminants; and (2) target compounds undergo biomagnification
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or biodilution in Great Lakes food web, depending on their physicochemical properties and biological
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half-life. Hence, we predict that biota from the lower Great Lakes (Lakes Ontario and Erie) would have
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higher concentrations due to the proximity to larger and more abundant municipal and industrial
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sources compared to the upper Great Lakes (Lakes Huron and Superior). Similarly, we predict that C4,
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C4C4, C8, C9andall target BZT-UVs will biodilute (i.e., Biomagnification Factor (BMF)1) due to longer
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biological half-life and higher estimated bioaccumulation factors (BAF) of these compounds in upper
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trophic level fish (Table 1).
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MATERIALS AND METHODS
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Samples. Sampling sites for the Great Lakes herring gull eggs and fish are shown in Figure 1.
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Fresh herring gull eggs were collected in 2014 from 7 colonies in Great Lakes under federal scientific
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permits. The sampling sites included: Granite Island (GI; n = 10; site 1) and Agawa Rocks (AR; n = 10;
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site 2) in Lake Superior, Chantry Island (CI; n = 10; site 3) in Lake Huron, Middle Island (MI; n = 10;
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site 4) and Port Colborne (PC; n = 10; site 5) in Lake Erie, Weseloh Rocks (WR; n = 6; site 6) in
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Niagara River, and Hamilton Harbour (HH; n = 10; site 7) in Lake Ontario.Lake Trout samples were
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collected from Thunder Bay-Pie Island (TB; n=5, 2013; site 1), Marathon (MT; n=5; 2014; site 2) and
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Whitefish Bay (WB; n=10; 2014; site 3) in Lake Superior, Goderich (GR; n=5; 2014; site 4) in Lake
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Huron, Dunkirk (DK; n=5; 2014; site 6) in Lake Erie, and Niagara-on-the-Lakein Lake Ontario(NL;
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n=5; 2014; site 7). In the western basin of Lake Erie, walleye occupy the top trophic level due to the
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relative shallow and warm conditions that are inhospitable to lake trout, and were sampled accordingly
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(EW; n = 5; 2014; site 5).The WB (2014) Lake Superior lake trout food web sampling consisted of
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pooled plankton (>153µm; extracted in triplicate), pooled mysis (Mysis relicta) (extracted in triplicate),
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slimy sculpin (Cottus cognatus; pooled from 20 fish, extracted in triplicate), rainbow smelt (Osmerus
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mordax; pooled from 12 fish, measured in triplicate) and deep water sculpin (Myoxocephalus
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thompsonii; 5 different pooled samples, consisting of 7 to 12 fish each). Though our previous data8
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indicated liver as the predominant site of accumulation in fish, whole body homogenate is the
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consistent
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arepublished22,24and briefly described in the Supporting Information (SI). The biological parameters of
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samples from the Great Lakes are shown in Table S2.
approach
for
studying
food
web
biomagnification.
Details
on
the
capture
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Chemicals, Sample Preparation and Instrumental Analysis. Detailed information of target
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SDPAs and BZT-UVs are shown in Table 1 and Figure S1.The details of other chemicals used in the
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experiment, sample preparation methods and instrumental analysis are previously published1-3and
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shown in SI (Table S3 and S4). The analyses of stable isotopes and fatty acids were based on published 7 Environment ACS Paragon Plus
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methods25-27 as shown in the SI.
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QA/QC. Glass materials were used in the experiment whenever possible to limit any possible
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background contamination. Procedural blanks (n = 2 for egg samples; n= 1 for other biota samples) and
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one spike-recovery sample (known amount of target compounds added to samples) were included for
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each batch of samples. The recovery of the target compounds in spike-recovery egg samples ranged
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from 68±26% (C9C9)to 112 ± 14% (diAMS) for SDPAs and from 74±11% (UV329) to 89±28%
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(UV234) (mean ± standard deviation (SD)) for BZT-UVs (Table S4).For fish and other biota samples,
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the recovery was in the range of 77±26% (C8C8) - 89 ± 21% (C8) and 73 ±18%(UV350)-78 ±17%
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(UV328)for SDPAs and BZT-UVs, respectively (Table S4). The method limits of quantification
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(MLOQs) were based on 3 times of standard deviation (SD) of the blanks (n= 6 for eggs; n = 12 for
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fish and other biota samples). For analytes which were not observed in the method blanks, standard
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concentration producing a signal with 10 times signal to noise ratio in acetonitrile were used to estimate
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the MLOQ. In egg samples, the MLOQs were in the range of 0.001-0.01 ngg-1 (ww) for SDPAs and
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0.03-0.66 ngg-1 (ww) for BZT-UVs (Table S4). The MLOQs in other biota samples were in the range
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of 0.001-0.014 and 0.03-1.4 ngg-1 (ww) for SDPAs and BZT-UVs, respectively (Table S4).All
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concentrations in samples were blank-subtracted.
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Data Analysis. Data were analyzed using R 3.3.1 (with RStudio 0.99.903) (Boston, MA, USA),
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GraphPad Prism 7.0 (La Jolla,CA, USA) and IBM SPSS Statistics (Version 23) to determine the
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existence of possible differences in SDPAs and BZT-UVs levels in different samples and affecting
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factors. Statistics for data with censored values (≤50% censoring and detects > 3) were conducted using
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the robust regression on order statistics (ROS) method in R by the Nondetects and Data Analysis
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(NADA) package (V1.5-6).28For the pooled samples (i.e., mixed plankton, mysis, slimy sculpin and
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rainbow smelt) with small sample size (n=3), the censored values were substituted by 1/2 MLOQ when
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contaminants were detected in two samples.28Concentration is reported as arithmetic mean±standard
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error unless otherwise indicated.Data (Shapiro-Wilk test) were logarithmically transformed to
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approximate a normal distribution before further statistical analysis. One-way ANOVA followed by
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Tukey’s test were used for comparisons. Significance level was set as p
