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Puget Sound Indicators
Contaminants in English sole
Basics
Healthy Water Quality
Toxics in Aquatic Life
Indicator
Contaminants in English sole
Vital Sign Indicator
Chemical Concentration Wet Weight (ng/g wet weight)
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By 2030, 95% of the samples gathered across Puget Sound habitats exhibit a declining trend of contaminant levels, or are below thresholds of concern for species or human health.

By 2050, 95% of the samples gathered across Puget Sound habitats exhibit contaminant levels below thresholds of concern for species or human health and show no increasing trends.

Target fact sheet

Louisa Harding
Louisa.Harding@dfw.wa.gov
Washington Department of Fish and Wildlife
Contributing Partners
Last Updated
7/1/2022 9:54:12 AM
Map
Description
The contaminants in English sole indicator measures chemical concentrations in fish fillets and disease occurrence in fish to assess impacts of contaminants in the benthic (seafloor) habitat. PCBs and PBDEs in fillets indicate contaminant levels people may be exposed to from eating benthic fish. Liver tumors and the presence of a female-specific protein, vitellogenin, in the blood of male fish indicate health impairments due to PAH and EDC exposure, respectively, in the benthic habitat.
Vital Sign Indicator Chart
Contaminant and disease levels in English sole from 12 index sites. For contaminants, red indicates high contamination, with some English sole (5th percentile or greater) exceeding the health thresholds and green indicates low contamination, with most English sole (95th percentile or greater) below the thresholds. For PAH- or EDC- related disease, red indicates significantly higher risk of disease compared to baseline, whereas green indicates no significantly elevated risk.

English sole is one of Puget Sound's most common and abundant benthic flatfishes. It lives in close contact with the seafloor, and feeds on organisms living in the sediments. Typically, English sole from distinct areas within Puget Sound (populations) spend the spring, summer, and part of the fall in predictable, relatively shallow foraging (feeding) areas (Day 1976, O’Neill et al., 2007). In winter months they migrate to deeper offshore areas to spawn, and then return to their foraging areas in the spring (Moser et al., 2013). During the winter months, English sole tend to eat much less (Day 1976), so the contaminant levels in their bodies mostly represent the foraging habitats where they are caught.

The abundance, local foraging behavior, and wide distribution of English sole make them ideal indicators of toxic chemical contaminants in Puget Sound's benthic (seafloor) habitat. PCB and PBDE concentrations in English sole fillet (muscle tissue) primarily address human health concerns. They indicate the contaminant-risk to people consuming Puget Sound flatfish, from chemical contamination in the benthic habitat. These contaminant levels in English sole are used by Washington Department of Health as a first step in evaluating whether fish are safe to eat and for establishing flatfish consumption advice. Liver disease and vitellogenin induction address fish health. They are linked to PAH and EDC contamination in the benthic habitat and they signify the negative health impacts English sole experience from exposure to these chemicals.

Key Vital Sign Indicator Results
  • The Contaminants in English sole indicator did not meet the recovery goal (see target description) because PCB levels in English sole fillet tissue exceeded the human health screening value and English sole males showed signs of EDC-related reproductive impairment at multiple Central and South Puget Sound locations. For detailed results, see the Interpretation of Results section.
  • PCB levels in English sole fillet tissue exceeded the human health threshold (i.e., the WA Department of Health (DOH) screening value concentration for subsistence fishers or high-level consumers) at nine out of twelve (75%) index sites. PCB levels have improved over the past 20 years for only one of those locations and continue to worsen at three locations (the Duwamish River, Everett, and Eagle Harbor).
  • English sole fillet PBDE concentrations were below the human health threshold at all 12 locations, and they are either holding steady or decreasing.
  • Liver disease resulting from exposure to PAHs has significantly declined at six index sites including Everett, Eagle Harbor, the Seattle Waterfront, the Duwamish River, Anderson Island, and Tacoma City Waterway. The risk of disease was 2.5 to 40 times higher at these sites compared to baseline in the mid-1990s and is no longer significantly elevated compared to background levels. The PAH 2020 recovery target was reached for all index sites as of 2019.
  • Male English sole from five out of 12 (42%) sites showed increased risk of expressing vitellogenin, suggesting an increased risk of reproductive impairment at these sites.
    • Vitellogenin is a protein involved in female reproductive development and is normally only expressed in mature females with developing eggs.
    • Vitellogenin expression in male fish is commonly used as an indicator of exposure to estrogenic chemicals in their environment.
    • Vitellogenin expression in male fish has previously been linked to adverse reproductive health in a variety of fishes.
  • Although there has been some improvement in the contaminants in English sole indicator (PAHs and PBDEs), PCB concentrations remain high in fish from urban and near-urban bays and EDC-related vitellogenin induction continues in both urban and non-urban (rural/residential) areas. These results suggest continued PCB and EDC inputs to Puget Sound, likely via stormwater runoff and wastewater effluent (EDCs). These sources will likely increase as the Puget Sound region population continues to grow.
Methods
Monitoring Program

Washington Department of Fish and Wildlife, Toxics Biological Observation System

Data Source

PCB and PBDE contaminant levels and time trends calculated from West et al. (2017) and from Washington Department of Fish and Wildlife, Toxics Biological Observation System unpublished data.

PAH-induced liver disease and EDC-induced vitellogenin odds ratios calculated from Washington Department of Fish and Wildlife, Toxics Biological Observation System unpublished data.

This update presents the most current contaminant levels and contaminant-related disease risk for English sole collected from twelve index monitoring locations, each representing a distinct population. These index sites were selected to cover a broad geographic area and a range of land-development from relatively undeveloped rural or residential (non-urban) to highly developed (urban or industrial). English sole are sampled using a bottom trawl in the spring (April to May) while they are feeding in their foraging grounds.

PCBs and PBDEs are measured directly in composite samples of 10 to 20 fish muscle tissue (fillet) of English sole (see West et al., 2017 for detailed analysis methods), as an indication of the levels of chemicals humans may be exposed to when they eat Puget Sound flatfish. PCB and PBDE concentrations in English sole fillet are compared to Washington Department of Health (DOH) Human health screening values for subsistence fishers or high-level consumers (8 ng/g wet weight for PCBs and 40 ng/g wet weight for PBDEs). Concentrations above these screening values trigger concern for DOH-defined high-level consumers (i.e., more than two servings per week) and are therefore considered above our recovery target for PCB and PBDE human health thresholds.

Summary statistics for PCBs and PBDEs are displayed in boxplots.

  • The line in the middle of the box shows the median PCB or PBDE concentration.
  • The top and bottom ends of the box show the 75th and 25th percentile of the data.
  • The top and bottom diamonds connected to the box by vertical whiskers show the 95th and 5th percentile, respectively.
  • The boxplots are color-coded red or green to indicate whether most of the samples, estimated by the 95th percentile, fell below (green) or above (red) the human health screening values.
  • The human health screening value is shown on the plot as a dashed horizontal line.

Ten of the twelve index locations had sufficient data to evaluate time trends in PCBs and PBDEs. Multiple linear quantile regression models (Cade and Noon 2003) were used to help interpret PCB and PBDE time trends. Trend analyses were focused on the upper boundary of the distribution of contaminant levels in each year (95th percentile), rather than an estimate of central tendency (e.g., the mean, or median). Using this method, we determined whether the highest values in each year were declining, increasing, or remaining unchanged. All regressions were conducted on log10-transformed data, which were back-transformed to plot geometric values. Since the quantile regressions were focused on the upper boundary of contaminant level distribution, they proved to be highly sensitive to extreme values in the datasets. As a result, survey years with a 95th percentile that greatly exceeded the remaining data points (i.e., outlier years) were removed from the time trend analysis (as indicated by asterisks on the time trend plot).

The quantile regressions provide statistics to help determine whether the 95th percentile concentration of POPs is increasing (a positive slope) or decreasing (a negative slope), whether the modeled trend is statistically significant (i.e., how confidently it can be distinguished from random events), and how strong the trend is (the annual rate of change). Fish age and the sex ratio of each composite sample were included in regressions as statistical covariates to help account for variability in the age and sex of sampled fish, which could influence contaminant levels. POPs accumulate as fish age in both males and females, but because English sole are known to segregate by sex (Becker, 1988) males and females may experience different exposure to contaminants. Covariates were excluded from the models if they were not significant explanatory factors. Quantile regression models with slope coefficient probability values <0.05 were considered statistically significant, or distinguishable from random events. Plotted trend lines (solid black lines) predict POP concentrations at the 95th percentile after adjusting for covariates. The gray areas around statistically significant trend lines represent the 95% confidence interval for the slope parameter calculated in the quantile regression. Confidence in a determination of whether English sole at a given location have fully reached the recovery target is greatest when the upper confidence boundary for the 95th percentile falls below the human health effects threshold.

Unlike PCBs and PBDEs which build up in fish tissues over time, PAHs are metabolized, or broken down inside the body of fish, making it difficult to assess ongoing levels of exposure. Although fish (and many other vertebrates) can metabolize PAHs, the metabolization process can cause disease, including the development of liver tumors (Myers et al. 1991). Therefore, instead of measuring PAH concentrations in English sole tissue, exposure of English sole to PAHs is measured by the presence of specific liver tumors that are known to be caused by PAH exposure (Myers et al., 2003). The presence of tumors in fish reveals the effects of long-term exposure to PAHs, rather than a short “snapshot” of PAH exposure that might be measured in their body. The ability to detect PAH-induced liver disease is a unique case where we can directly measure health impacts in fish (i.e., disease) resulting from contaminant exposure.

The clean reference value for PAHs represents the level of background liver disease exhibited by English sole from relatively uncontaminated areas. This clean reference value is set to one, and the results for liver disease in all other English sole are calculated as the odds of developing liver disease, compared to the clean reference area. For example, if the odds ratio for liver disease at Eagle Harbor is 2.5, fish living there are 2.5-times more likely to develop this PAH-disease than fish living in the clean reference condition. Because the odds of developing this liver disease also increases with age (even in uncontaminated areas), odds ratios are corrected by fish age at all sites using multiple logistic regression.

To assess trends in PAH-induced liver disease over time, the age-adjusted odds ratios were analyzed by linear regression across time for each site. Linear regression models with slope coefficient probability values <0.05 were considered statistically significant. Plotted trend lines (solid black lines) predict the age-adjusted odds ratios for developing liver disease at a given site and the gray areas around statistically significant trend lines represent the 95% confidence interval for the slope parameter.

EDC-related reproductive impairment of English sole was first observed in Puget Sound more than 20 years ago. These observations included expression of vitellogenin in male English sole and altered reproductive timing in female English sole from several urban sites (Johnson et al. 2008). Vitellogenin is an egg-yolk protein produced in the liver of fish and other egg-laying animals that is normally only expressed in sexually mature females with developing eggs. However, vitellogenin can be induced in male or immature fish when they are exposed to environmental chemicals with estrogen-like activity. As a result, vitellogenin induction in male fish is commonly used as an indicator of exposure to EDCs, and specifically to estrogenic chemicals (Sumpter and Jobling, 1993). Similar to PAH-induced liver disease, the ability to measure EDC-induced vitellogenin in male fish means we can directly measure a biological response to estrogenic chemicals. Furthermore, vitellogenin-induction has been associated with other symptoms of reproductive impairment including decreased gonad size, and reduced fecundity and fertility such that vitellogenin expression in males may be considered a warning sign of adverse reproductive consequences (Cheek et al., 2001; Kime et al., 1999).

In 2017, WDFW established new methods for measuring vitellogenin in male English sole for use in the contaminants in English sole indicator reporting. The clean reference value for EDC-induced vitellogenin expression in males from uncontaminated areas is set to one, and the results for vitellogenin expression in all other male English sole is calculated as the odds of expressing vitellogenin compared to the clean reference area (as an odds ratio). For example, if the odds ratio of vitellogenin induction at Seattle Waterfront is 20, it is 20 times more likely for a male fish living at the Seattle Waterfront area to express vitellogenin than fish living in uncontaminated areas.

To support the vitellogenin data, WDFW also measures the presence of natural estrogens (e.g., estradiol) and chemicals that mimic estrogen (e.g., bisphenol-A) in the bile of English sole. These EDCs represent a large group of chemicals that may cause reproductive impairment, and their presence in the fish’s bile indicates a recent exposure. WDFW also monitors the reproductive status of both male and female English sole to identify potential alterations in their reproductive timing that may result from exposure to EDCs. These alterations in reproductive state may provide evidence of more severe reproductive disruption in these fish.

Critical Definitions
  • Polychlorinated biphenyls (PCBs) are a group of synthetic (man-made) chemicals consisting of 209 compounds, or congeners, each containing a unique number and position of chlorine atoms attached to two phenyl (aromatic) rings. These typically oily compounds were designed for various industrial and residential products and uses (electrical transformers, cable insulation, caulking and plastics) and consist of complex mixtures of congeners. PCBs were largely banned in the US by 1979, but they are still found in materials produced before the ban, as unintentional byproducts of manufacturing, and in small amounts (<50 parts per million), still allowed in new products. PCBs are classified as a Persistent Organic Pollutant (POP), because they are resistant to most forms of degradation, and once released to the environment, they can bioaccumulate in organisms and cause adverse health impacts in wildlife and humans.
  • Polybrominated diphenyl ethers (PBDEs) are a group of synthetic (man-made) chemicals consisting of 209 compounds, or congeners (similar to PCBs), although each containing a unique number and position of bromine atoms surrounding two phenyl-ether rings. PBDEs were designed primarily as flame-retardants to prevent or slow the spread of fire in products ranging from electronics and furniture to clothing. In 2008, Washington state banned the sale of select PBDE mixtures, however they can still be found in materials produced before the ban. PBDEs are classified as a POP, because once released to the environment are resistant to degradation, bioaccumulate in organisms and have adverse health impacts in wildlife and humans.
  • Polycyclic aromatic hydrocarbons (PAHs) are a group of chemicals composed of carbon and hydrogen molecules arranged in multiple aromatic rings. PAHs are naturally occurring chemicals found in coal and oil deposits and can enter the aquatic environment through air deposition from the incomplete combustion of organic material and fossil fuels (e.g., wood burning, forest fires, vehicle exhaust emissions, or coal fired power plants), surface runoff (e.g., oil leaks and spills), and in-water point sources (e.g., creosote treated pilings). Like POPs, PAH exposure has been linked to cancer and other adverse health impacts in wildlife and humans. However, unlike PCBs and PBDEs, PAHs can be metabolized by vertebrate species and therefore do not tend to bioaccumulate in fish. Invertebrate species, on the other hand, have limited ability to metabolize PAHs which can result in PAH accumulation in some species.
  • Endocrine disrupting compounds (EDCs) are chemicals capable of disrupting normal hormone levels or activity in humans or wildlife, resulting in altered behavior, reproduction, growth, metabolism or normal homeostasis (Crisp et al, 1998). Many EDCs act as estrogen mimics and can interfere with the reproductive system of exposed animals. One example, the synthetic estrogen 17α-ethynylestradiol (EE2) used in the birth control pill, is intended to interfere with reproduction in women taking it. However, EE2 and other natural estrogens can enter the aquatic environment through wastewater effluent and disrupt normal hormone signaling and reproduction in fish and other species. Some POPs and other industrial compounds (e.g., the plasticizer bisphenol-A) have also been shown to act as estrogen mimics and to disrupt normal reproduction in wildlife.
  • Vitellogenin (Vtg) is an egg-yolk protein precursor produced by the liver of female fish and other egg-laying animals. Normally, Vtg is produced in females during maturation in response to rising estradiol levels associated with normal reproduction. However, Vtg expression can also be stimulated in male or sexually immature fish in response to environmental exposure to endocrine disrupting chemicals (EDCs) that mimic estrogens. Since males do not normally produce high levels of estradiol, the presence of Vtg in their liver or blood indicates exposure to estrogenic chemicals in their environment. As a result, Vtg is widely used to monitor the presence of estrogenic chemicals in aquatic organisms (Sumpter and Jobling, 1993).
Interpretation of Results

Although there has been some improvement in the contaminants in English sole indicator, the 2020 recovery target has not been met because PCB concentrations and EDC-related vitellogenin expression in male fish remain high in many areas. At most locations, PCBs in English sole exceeded the human health threshold (8 ng/g wet weight) based on DOH screening levels considered protective of human health, with highest concentrations occurring in urban and near-urban locations in Central and South Puget Sound. Moreover, PCBs continue to increase in English sole from several sites. In contrast, PBDEs in English sole from all sampling locations fell below the human health threshold (40 ng/g wet weight), and they are either stable or decreasing at all locations.  

The spatial variation in contaminant concentrations suggest low PCB inputs in North Puget Sound (Strait of Georgia and Vendovi Island) and Hood Canal and higher inputs of contaminants in Central and South Puget Sound, particularly around urban or industrial bays and estuaries (Figure 1). English sole from North Puget Sound and in Hood Canal were relatively clean, with levels of PCBs below the human health threshold. These sites likely represent a best-case scenario for PCBs in the Puget Sound benthic habitat. In contrast, concentrations of PCBs in nearly all English sole from the remaining Central and South Puget Sound (including Whidbey Basin) sites exceeded the human health threshold for PCBs. Anderson Island and Carr Inlet were originally selected as clean reference sites for South Puget Sound, but it is clear PCBs have entered the benthic habitat there, despite their being relatively rural areas. Within Central and South Puget Sound, PCBs were greatest near more urbanized or industrialized areas including the Duwamish River, Seattle Waterfront, and Tacoma City Waterway. This is consistent with contaminants in juvenile chinook salmon, where we see PCB concentrations in fish from the Snohomish, Duwamish, Puyallup, and Nisqually rivers (and Lake Washington) exceeding the fish health threshold.

There were similar patterns of PBDEs in English sole, with highest concentrations occurring around urban areas (Duwamish River, Seattle Waterfront, and Tacoma City Waterway; Figure 1). However, PBDEs from all sampling locations in Puget Sound fell well below the human health threshold (40 ng/g wet weight) indicating that they are of lower concern in the benthic ecosystem. These patterns are consistent with the other Toxics in Fish Vital Sign indicators, especially contaminants in adult Chinook salmon and contaminants in Pacific herring where PBDE concentrations were lower than PCBs and fell well below health thresholds.

Figure 1: PCB and PBDE concentrations in fillet tissue of English sole collected from 12 locations throughout Puget Sound in 2019. Boxplots are colored green or red depending on whether they were below or above the WA Department of Health’s human health screening value for PCBs (8 ng/g wet weight) and PBDEs (40 ng/g wet weight; screening value not shown due to y-axis scale).

 

Evaluation of PCB, PBDE, and PAH time trends in English sole provides insight into progress towards reaching recovery targets (there is insufficient data to evaluate time trends of EDCs yet). The following graphs show PCB and PBDE contaminant concentrations over the past 20 years (Figures 2 and 3), and PAH-related liver disease over the last 30 years (Figure 5), for fish from the 10 long-term TBiOS index monitoring sites.  

English sole PCB concentrations have remained above the human health threshold for subsistence fishers or high-level consumers for the last 25 years in much of Puget Sound, particularly Central and South Puget Sound (Figure 2). The highest PCB concentrations have significantly increased from the late 1990s to 2019 at Everett, Duwamish River, and Eagle Harbor (~2% increase per year). A similar increasing trend in the highest PCB concentrations is apparent at Seattle Waterfront, but the trend is not significant at an alpha level of 0.05 (p = 0.087). PCBs in English sole from the Tacoma City Waterway peaked in 2003, and have since leveled off at a relatively high concentration. One notable exception to the increasing or high-yet-stable PCB concentrations observed at urban or industrial areas is Bremerton, where PCB levels have significantly declined in English sole since the late 1990s and early 2000s. Despite this improvement, PCBs in all English sole from Bremerton in 2019 continued to exceed the human health threshold.

PCBs in English sole from non-urban sites in North Puget Sound (Strait of Georgia and Vendovi Island) remained below the human health threshold and showed no significant change across time. English sole from Hood Canal were near the PCB human health threshold, however, the highest PCB concentrations measured from Hood Canal are not significantly increasing and were below the human health threshold in the last two survey years.

Figure 2: Trends in PCB concentrations in muscle tissue (fillet) of English sole collected from 10 index sites from the late 1990s through 2019. Solid black lines indicate significant trends (p < 0.05) in the 95th quantile of PCB concentrations over time as determined by multiple linear quantile regression. Dark shaded gray areas indicate the 95% confidence interval of significant trendlines. Dotted black trend lines indicate non-significant trends (p > 0.05) and are only displayed for visualization purposes. The boxplot for each year is color coded depending on whether most (95th percentile) of the samples exceeded (red) or met (green) the human health threshold of 8 ng/g wet weight (black dashed line). Blue asterisks indicate when a year was omitted from time trend analysis.

 

In contrast to PCBs, PBDE concentrations in English sole muscle tissue have been below the human health threshold at all locations since PBDE monitoring began in 2005 and there is no evidence to indicate that PBDEs are increasing in English sole from any site (Figure 3). These data suggest that PBDEs have not been a contaminant of great concern in the Puget Sound benthic ecosystem for at least the last 15 years. Despite already low levels, PBDEs are decreasing at two locations, Tacoma City Waterway and Bremerton. PBDEs in English sole from Tacoma City Waterway which were among the highest levels when measurements began in 2005, have declined almost 3% per year.

Figure 3: Trends in PBDE concentrations in muscle tissue (fillet) of English sole collected from 10 index sites from the late 1990s or early 2000s through 2019. Solid black lines indicate significant trends (p < 0.05) in the 95th quantile of PBDE concentrations over time as determined by multiple linear quantile regression. Dark shaded gray areas indicate the 95% confidence interval of significant trendlines. Dotted black trend lines indicate non-significant trends (p > 0.05) and are only displayed for visualization purposes. Each boxplot is color coded green, indicating that most (95th percentile) of the samples met the human health threshold of 40 ng/g wet weight in each year and location (threshold not displayed due to y-axis range). Blue asterisks indicate when a year was omitted from time trend analysis.

 

Evaluation of PAH-related liver disease and EDC-related reproductive impairment provide direct measures of contaminant related impacts to English sole health, and potentially other species in benthic habitats. Such effects-based monitoring can be especially useful when the contaminants are quickly metabolized and do not build up in fish tissue (e.g., PAHs and some EDCs) or when the precise suite of chemicals responsible for biological effects is unknown or may differ between locations (EDCs).

Figure 4 shows the risk of fish developing PAH-induced liver disease across 12 locations. In 2019, all English sole index sites met the 2020 target value for PAHs, with no evidence of elevated risk of liver disease compared to baseline conditions. This represents a dramatic improvement from historical conditions at several locations. 

Figure 4: Risk of PAH-induced liver disease in English sole from 2019. Risk was calculated as odds ratios using logistic regression with age as a covariate. Error bars show 95% confidence intervals for the odds ratio estimate. Diamonds are color coded green if the odds ratio for a site was not significantly different from the clean reference background condition of one (dashed line).

 

The likelihood of PAH-induced liver disease peaked in the mid-1990s throughout Puget Sound, particularly at urban and near-urban sites (Figure 5). The age-adjusted risk of English sole developing liver disease has significantly declined at 6 of the 10 sites and have remained low at the remaining 4 sites. For example, odds ratios of liver disease in fish from Elliott Bay, Eagle Harbor, and Duwamish River were 9, 15 and 41 times higher in the mid-1990s compared to fish from clean reference areas, respectively.

 

In 2019, male English sole from Port Madison, Elliott Bay, Duwamish River, Tacoma City Waterway, and Carr Inlet had 7, 20, 6, 7, and 12 times higher odds of expressing vitellogenin, respectively, than males from clean reference sites (Figure 6). These odds ratio values correspond to 23 to 52% of males from those sites expressing vitellogenin, whereas at northern non-urban stations (Strait of Georgia, Vendovi Island, and Hood Canal) 0 to 8% of male fish had measurable vitellogenin levels. Vitellogenin induction in male fish is associated with environmental exposure to estrogenic chemicals, particularly natural and synthetic estrogens present in sewage or wastewater treatment plant effluent (Desbrow et al., 1998, Sumpter and Jobling, 1993). However, the sources of EDC exposure in Puget Sound may differ across sites.

Although our methods for measuring vitellogenin in English sole have changed over the last 20 years, many of the locations with elevated occurrence of vitellogenin induction in males have remained consistent. In the late 1990s and early 2000s, a higher prevalence of vitellogenin expression in male English sole was observed at three sites in Elliott Bay ranging from 38-47% vitellogenic males and at Tacoma City Waterway with 22% vitellogenic males (Johnson et al., 2008). Furthermore, in 2019, male English sole from Elliott Bay had the highest concentrations of vitellogenin across all sites (data not shown), which is consistent with past data (Johnson et al., 2008). 

Female English sole may also be affected by exposure to estrogenic chemicals or other EDCs. Although not included in the EDC indicator, we also monitor the reproductive status of female English sole as further evidence of potential impacts of EDCs on English sole reproduction. We sample English sole in the spring, following their winter spawning when we expect females to be in a “post-spawning” state. In general, female English sole throughout Puget Sound follow this pattern with most females in a post-spawning state in the spring, and some in a maturing stage of development in preparation for the following spawning season (Figure 6). However, a high proportion of females were in a ripe or spawning state at Elliott Bay and Carr Inlet – the two locations with the highest risk of vitellogenin expression in males – supporting the conclusion that these areas are contaminated with estrogenic chemicals.

Figure 6: Top panel: Risk of EDC-induced vitellogenin expression in male English sole from 2019. Risk was calculated as odds ratios using logistic regression. Error bars show 95% confidence intervals for the odds ratio estimate. Diamonds are color coded based on whether the odds ratio for a site was significantly different (red) or not (green) from the clean reference background condition (dashed line). Bottom panel: Percent of female English sole from 2019 at 3 broad reproductive stages (Blue = post-spawning, Green = maturing, Red = ripe or spawning condition).

 

Although not included in the EDC indicator, direct measurements of estrogenic chemicals including natural estrogens (e.g., estradiol) and industrial chemicals with estrogenic activity (e.g., bisphenol-A) in bile of male fish provide additional information to explain symptoms of impaired reproduction observed in Puget Sound. Estrogenic chemicals, particularly natural estrogens, measured in male English sole bile were highest at Carr Inlet followed by Elliott Bay, supporting a hypothesis that such chemicals play a role in the reproductive impairment observed at these locations (da Silva et al., 2013; unpublished data).Together these data suggest that male and female English sole from urban as well as non-urban bays in Central and South Puget Sound are exposed to estrogens or estrogen-like chemicals that may be disrupting their reproduction.

Although we are currently only monitoring EDC-related reproductive impairment in English sole, past research suggests that other species may be similarly impacted. For example, juvenile chinook salmon collected in Duwamish River and Elliott Bay had significantly elevated vitellogenin levels compared to control fish (Peck et al., 2010).

 

PCBs: Despite bans prohibiting the intentional manufacture and sale of PCBs in the US and many other countries in 1979, and considerable mitigation efforts to reduce PCB contamination in several urban bays, there remains broad PCB contamination in the benthic ecosystem of Central and Southern Puget Sound. Indeed, PCB concentrations in English sole continue to increase at more locations than they are decreasing. This continued contamination is consistent with the persistent nature of these chemicals. Benthic fish like English sole bioaccumulate PCBs from prey living in contaminated sediments, and the chemicals recirculate throughout the complex predator-prey linkages in the benthic food web. PCBs also continue to enter the marine and estuarine waters of Puget Sound from watershed sources, primarily via surface runoff (also called stormwater) (Osterberg and Pelletier, 2015). In a regional analysis National Pollutant Discharge Elimination System (NPDES) stormwater permits, Hobbs et al. (2015) reported the highest PCB levels from permitted stormwater dischargers located in industrial and commercial watersheds, which is consistent with the pattern we observed in English sole.  Any reduction of PCBs in marine sediments may be offset by such ongoing watershed sources.

PBDEs: PBDEs occurred in English sole at approximately 1/30th the concentration of PCBs, on average, and there was no increasing trend in PBDEs at any location. However, trends data for PBDEs in English sole are only available from 2005, so earlier conditions remain unknown. In any case, the lack of any increasing trend in English sole PBDEs from any location suggests PBDE control measures, including both statutory and voluntary controls on PBDE production and use in Washington State may have prevented significant PBDE contamination of benthic food webs throughout Puget Sound.

PAHs: Much progress has been made in reducing the effects of cancer-causing PAHs on fish health in Puget Sound. Reduction of PAHs in Eagle Harbor English sole resulted from directed superfund cleanup and control activities. Reductions in PAH-induced liver disease at other sites, including Seattle Waterfront, Duwamish River, and Tacoma City Waterway, likely benefitted from a wide range of recovery actions including removal of creosote-treated pilings and contaminated sediments, and watershed source controls.

EDCs: Although WDFW began monitoring EDC-related reproductive impairment in English sole more than 20 years ago, changes in methodology and long gaps in monitoring prevent direct assessment of changes in EDC-exposure over time. However, we can expect that local and regional changes in wastewater treatment may contribute to trends in EDC exposure and related health effects in fish. At Seattle Waterfront, where the strongest evidence of EDC-related reproductive impairment in English sole exists, various actions have been taken to reduce EDC inputs including increased wastewater treatment capacity and stormwater holding tanks to reduce combined sewer overflow events. However, since 2000, the Puget Sound region’s population has increased by over 4 million people, with much of that growth in King County. Wastewater treatment can reduce estrogenic chemicals in effluent but does not eliminate them completely and the efficiency of EDC removal varies considerably based on the wastewater treatment processes (Duan et al., 2021). Therefore, with increased population comes increased wastewater effluent entering Puget Sound, and the potential for increased EDC exposure. In Carr Inlet, a relatively lightly populated area, the source of estrogenic chemicals is less clear, raising questions regarding the origin of EDCs in that water body. Regardless of the source, there is evidence that steroidal estrogens, thought to be a major driver in EDC-related reproductive impairment, may accumulate in sediments near wastewater treatment plants outfalls, combined sewer overflow outfalls, and septic systems in the watershed, potentially resulting in a persistent source of estrogenic contaminants to benthic organisms (Peck et al., 2004).

 

The four chemical groups in the Toxics in Fish Vital Sign were chosen because they were widely known to occur in Puget Sound or other similar ecosystems. In addition, these four groups represent a wide range of chemical properties (persistent vs non-persistent) and contamination conveyance pathways or sources (e.g. stormwater vs wastewater effluent) likely requiring different remediation strategies.

A wide range of activities and actions have taken place, are underway, or are planned to address these chemicals. Planned activities include usage bans, Superfund Site cleanups, sediment remediation and source monitoring and control such as combined sewer overflow reductions. A current evaluation of human activities that contribute to these chemicals in Puget Sound has been completed by the ongoing Stormwater Strategic Initiative, as well as a prioritization of actions to be funded in the near term to reach the recovery goals defined above.

Please see Implementation Strategies outlined in Toxics in Fish Implementation Strategies to learn more about the development process.

Becker, D.S. 1988. Relationship between sediment character and sex segregation in English sole, Parophrys vetulus. Fishery Bulletin, 86(3), pp.517-524.

Cheek, A.O., Brouwer, T.H., Carroll, S., Manning, S., McLachlan, J.A. and Brouwer, M. 2001., Experimental evaluation of vitellogenin as a predictive biomarker for reproductive disruption. Environmental Health Perspectives, 109(7), pp.681-690.

Crisp, T.M., Clegg, E.D., Cooper, R.L., Wood, W.P., Anderson, D.G., Baetcke, K.P., Hoffmann, J.L., Morrow, M.S., Rodier, D.J., Schaeffer, J.E. and Touart, L.W., 1998. Environmental endocrine disruption: an effects assessment and analysis. Environmental health perspectives, 106(suppl 1), pp.11-56.

da Silva, D.A., Buzitis, J., Reichert, W.L., West, J.E., O’Neill, S.M., Johnson, L.L., Collier, T.K. and Ylitalo, G.M., 2013. Endocrine disrupting chemicals in fish bile: A rapid method of analysis using English sole (Parophrys vetulus) from Puget Sound, WA, USA. Chemosphere, 92(11), pp.1550-1556.

Day, D.E., 1976. Homing behavior and population stratification in central Puget Sound English sole (Parophrys vetulus). Journal of the Fisheries Board of Canada, 33(2), pp.278-282.

Desbrow, C.E.J.R., Routledge, E.J., Brighty, G.C., Sumpter, J.P., and Waldock, M., 1998. Identification of estrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitro biological screening. Environmental Science & Technology, 32(11), pp.1549-1558.

Duan, S., Iwanowicz, L.R., Noguera-Oviedo, K., Kaushal, S.S., Rosenfeldt, E.J., Aga, D.S. and Murthy, S., 2021. Evidence that watershed nutrient management practices effectively reduce estrogens in environmental waters. Science of the Total Environment, 758, p.143904.

Hobbs, W., Lubliner, B., Kale, N., and Newell, E. 2015. Western Washington NPDES Phase 1 Stormwater Permit: Final S8.D Data Characterization 2009-2013, Washington State Department of Ecology: 154.

Johnson, L.L., Lomax, D.P., Myers, M.S., Olson, O.P., Sol, S.Y., O’Neill, S.M., West, J. and Collier, T.K., 2008. Xenoestrogen exposure and effects in English sole (Parophrys vetulus) from Puget Sound, WA. Aquatic Toxicology, 88(1), pp.29-38.

Kime, D.E., Nash, J.P. and Scott, A.P., 1999. Vitellogenesis as a biomarker of reproductive disruption by xenobiotics. Aquaculture, 177(1-4), pp.345-352.

Moser, M.L., Myers, M.S., West, J.E., O'Neill, S.M., and Burke, B.J., 2013. English sole spawning migration and evidence for feeding site fidelity in Puget Sound, USA, with implications for contaminant exposure. Northwest Science, 87(4), pp.317-325.

Myers, M. S., Landahl, J.T., Krahn, M.M., and McCain, B.B. 1991. Relationships between hepatic neoplasms and related lesions and exposure to toxic chemicals in marine fish from the U.S. West Coastal. Environmental Health Perspectives 90:7-15.

Myers, M.S., Johnson, L.L. and Collier, T.K., 2003. Establishing the causal relationship between polycyclic aromatic hydrocarbon (PAH) exposure and hepatic neoplasms and neoplasia-related liver lesions in English sole (Pleuronectes vetulus). Human and Ecological Risk Assessment, 9(1), pp.67-94.

O’Neill , S.M., Moser, M.L., Myers, M.S., Quinnell, S.R., and West, J.E., 2007. Acoustic telemetry reveals daily movement patterns and annual homing migration to foraging habitats by English sole: application to management of contaminated sediments. Proceedings of the 2007 Puget Sound Georgia Basin Research Conference.

Peck, M., Gibson, R.W., Kortenkamp, A. and Hill, E.M., 2004. Sediments are major sinks of steroidal estrogens in two United Kingdom rivers. Environmental Toxicology and Chemistry: An International Journal, 23(4), pp.945-952.

Peck, K.A., Lomax, D.P., Olson, O.P., Sol, S.Y., Swanson, P. and Johnson, L.L., 2011. Development of an enzyme-linked immunosorbent assay for quantifying vitellogenin in Pacific salmon and assessment of field exposure to environmental estrogens. Environmental Toxicology and Chemistry, 30(2), pp.477-486.

Servos, M.R., Bennie, D.T., Burnison, B.K., Jurkovic, A., McInnis, R., Neheli, T., Schnell, A., Seto, P., Smyth, S.A. and Ternes, T.A., 2005. Distribution of estrogens, 17β-estradiol and estrone, in Canadian municipal wastewater treatment plants. Science of the Total Environment, 336(1-3), pp.155-170.

Sumpter, J.P. and Jobling, S., 1995. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environmental health perspectives, 103(suppl 7), pp.173-178.

West, J.E., O’Neill, S.M. and Ylitalo, G.M., 2017. Time trends of persistent organic pollutants in benthic and pelagic indicator fishes from Puget Sound, Washington, USA. Archives of environmental contamination and toxicology, 73(2), pp.207-229. 

O'Neill, S.M. and J.E. West. 2007. Persistent Bioaccumulative Toxics in the Food Web. Pages 140-148; 151-156 in Puget Sound Action Team, editors. 2007 Puget Sound Update: Ninth Report of the Puget Sound Assessment and Monitoring Program. Washington Department of Fish and Wildlife; Publication Number PSAT 07-02. Olympia, Washington. 276pp. http://wdfw.wa.gov/publications/01051/  

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