Predictors of mercury spatial patterns in San Francisco Bay forage fish

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Predictors of mercury spatial patterns in San Francisco Bay forage fish

Ben K. Greenfield * , Darell G. Slotton , Katherine H. Harrold

Accepted for publication on July 22, 2013

Environmental Toxicology and Chemistry

http://onlinelibrary.wiley.com/journal/10.1002/%28ISSN%291552-8618

San Francisco Estuary Institute, Richmond, CA, USA

Environmental Health Sciences Division, School of Public Health, University of California - Berkeley, CA, USA

Department of Environmental Science and Policy, University of California - Davis, CA, USA

Current address: Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North

Carolina - Chapel Hill, NC, USA

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* Address correspondence [email protected]

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mailto:[email protected]:[email protected]:[email protected]


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ABSTRACT

Pollution reduction efforts should be targeted towards those sources that result in the

highest bioaccumulation. For mercury (Hg) in estuaries and other complex water bodies,

carefully designed biosentinel monitoring programs can help identify predictors of

bioaccumulation and inform management priorities for source reduction. We employed a

probabilistic forage fish Hg survey with hypothesis testing in San Francisco Bay. The study goal

was to determine what pollution sources, regions, and landscape features were associated with

elevated Hg bioaccumulation. Across 99 sites, whole body Hg concentrations in Mississippi

silversides (Menidia audens) and topsmelt (Atherinops affinis) followed a broad spatial gradient,

declining with distance from the Guadalupe River (Pearsons r= -0.69 and -0.42), which drains

historic mining areas. Site landscape attributes and local Hg sources had subtle effects which

differed between fish species. Topsmelt Hg increased in embayment sites (i.e., enclosed sites

including channels, creek mouths, marinas, and coves) and sites with historic Hg contaminated

sediment, suggesting an influence of legacy industrial and mining contamination. In 2008,

Mississippi silverside Hg was reduced at sites draining wastewater treatment plants. Fish Hg was

not related to abundance of surrounding wetland cover but was elevated in some watersheds

draining from historic Hg mining operations. Results indicated both regional and site-specific

influences for Hg bioaccumulation in San Francisco Bay, including legacy contamination and

proximity to treated wastewater discharge.

Keywords: Mercury, Prey fish, Estuary, Biosentinel, Bioaccumulation

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INTRODUCTION

Mercury (Hg) is a global pollutant that adversely impacts ecosystems and human health.

Global Hg concentrations are elevated due to widespread human use and inadvertent release,

creating a need for coordinated efforts to curtail Hg release, transport, and exposure [1].

Anthropogenic Hg sources to estuarine and coastal ecosystems include runoff from Hg and gold

mining operations, atmospheric emissions (e.g., coal combustion), and point sources associated

with historic or current industrial activity [1-5]. Methylmercury (MeHg) is highly toxic and

bioaccumulative [6], triggering reproductive effects in wildlife [7] and potential developmental

and neurological effects to humans [8, 9]. At the regional scale, carefully designed research and

monitoring is needed to prioritize MeHg management actions in the presence of multiple

spatially-distributed sources.

Comparative studies of MeHg in forage fish (small, short-lived prey fish, consumed by

piscivorous wildlife) aid in describing spatiotemporal patterns and explanatory variables for

MeHg food web accumulation [10-18]. Forage fish integrate exposure across a several month

time period, and have limited ranges in age, diet, and movement area [17]. Thus, forage fish are

often used to describe spatial patterns in food web MeHg, and the factors that contribute to

elevated MeHg [10-13, 18]. However, probabilistic spatial surveys and hypothesis testing

approaches are rarely employed to evaluate forage fish contamination within a single water body.

San Francisco Bay (the Bay) is influenced by Hg watershed loads and sediment deposits

from historic mining operations and industrial sources, making it an important system for

characterizing ecosystem MeHg exposure [3, 19-21]. Local sources targeted for management

reduction include Hg mines, stormwater runoff from urban and industrial watersheds, municipal

publically owned wastewater treatment works (POTWs), drainage from the Central Valley

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watersheds, and industrial facilities [3, 22]. Historic Bay sediment contamination also contributes

Hg to the water column and food web [23-25]. As in other estuaries, the spatiotemporal

dynamics of MeHg concentrations, bioavailability, and bioaccumulation in the Bay are

influenced by complex biogeochemical factors, including variable primary productivity and

sulfate reduction, in addition to spatial differences in Hg loading [26-29]. Due to this

biogeochemical and spatial complexity, the relative importance of different source categories for

Hg bioaccumulation is poorly understood.

In addition to sources, there are several spatial factors that may influence MeHg

bioaccumulation within the Bay. Bay sediment and biota Hg are elevated in proximity to a

historic Hg mining district (New Almaden Mining District), in salt ponds and other semi-

enclosed embayments, and in interior wetlands [3, 13, 30-32]. Wetlands are frequently sites of

MeHg production, and consequently sources to adjacent ecosystems and biota [33-36]. Enclosed

environments, channels, and freshwater tributaries are also frequently associated with increased

MeHg in water, sediment, and biota [26, 37-40], due to the combined effects of watershed Hg

loading, legacy industrial sources, elevated organic carbon deposition, and spatial variation in

biota diets [4, 37, 41-43]. Forage fish sampling could indicate whether proximity to wetlands or

embayment areas (such as enclosed marinas, backwater sloughs, stream drainages, and natural

coves) predicts differences in biotic MeHg exposure within an estuary.

We report Hg spatial patterns in Bay forage fish collected from 99 sites between 2008

and 2010. Unlike many ambient monitoring programs, the study design was hypothesis-based.

Monitoring strata were defined, selected, and randomly subsampled to identify what kinds of

locations within the Bay exhibit elevated Hg concentrations in forage fish. Since MeHg is the

predominant Hg form in these fish [13], analyses of total Hg is assumed to indicate MeHg. Four

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questions are addressed: (1) What are the spatial trends in Bay forage fish Hg? (2) Are Hg

concentrations elevated in embayments, relative to open water sites within the Bay? (3) Does the

extent of fringing wetland habitat correlate with Hg concentrations? (4) Are concentrations

elevated at potential Hg source sites, relative to randomly selected sites? In addition to randomly

selected sites, 4 types of source sites were evaluated: sites draining watersheds impacted by

historic Hg mining (mine sites), sites draining urbanized and industrial watersheds (industrial

watershed sites), sites receiving treated effluent from wastewater treatment facilities (POTW

sites), and sites known to have elevated sediment Hg (contaminated sediment sites).

METHODS

Study design and site selectionThe study employed a stratified sampling design, intended to evaluate the 4 study

questions based on a priori hypotheses (Supplemental Data Text). The sample design included 99

sites distributed along the entire shoreline of San Francisco Bay from Lower South Bay to

Suisun Bay (Supplemental Data, Figure S1). Wetland channels and estuarine tributaries were

included but salt ponds and tidal lakes were excluded. Sites were probabilistically selected from

this sample frame using a Generalized Random Tessellation Stratified (GRTS) spatially balanced

sampling design [44]. Two sample draws were performed: the first was for random locations

across the entire Bay shoreline, and the second was from all identified points within the 4 source

categories, treating each category as a stratum.

The random sample draw included 2 categories (i.e., strata): open water sites (N= 25

sites) and embayment sites (N= 23 sites; Supplemental Data, Figure S2). The source sample

draw included 4 categories: Hg mine creeks (N= 4 sites), watersheds draining urban and

industrial areas (N= 13), POTW drainages (N= 7), and areas with relatively elevated sediment

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THg or MeHg (N= 15). For each subcategory, appropriate sampling locations were identified

using GIS, literature, and unpublished data (further detailed in Supplemental Data Text). Due to

limited sample sizes for POTWs and Hg mine sites, all sites within these categories were

sampled. To ensure sufficient coverage of wetland habitats, 12 additional sites adjacent to

nearshore wetlands were sampled in 2008, including 6 sites fringing the South Bay and 6 sites

fringing San Pablo and Suisun Bays (Supplemental Data Text). These wetland sites were only

included in the analysis of fringing wetland habitat versus fish Hg.

Fish samplingAll fish sampling was performed by beach seine in 2008, 2009, and 2010. To minimize

confounding seasonal variation with spatial variation, study analysis was restricted to the fall

season (August 27 to November 30 of each year). The target species were topsmelt (Atherinops

affinis; target total lengths of 60 - 100 mm) and Mississippi silverside (Menidia audens; target

total lengths of 40 - 80 mm), both of which have been successfully employed in the Bay as Hg

biosentinels [13, 16, 25]. Four composites of 5 individuals each per species were targeted for

total Hg at each sampling event. Target composites each included similar-sized individuals, with

the composites distributed in ascending 10 mm size windows spanning the overall size range

targeted for each species (i.e., for Mississippi silverside: composite 1,N= 5 at 40 - 50 mm

through composite 4,N= 5 at 70 - 80 mm).

For the Bella Oaks and Borges Hg mine sites, target species were not available. At these

2 sites, prickly sculpin (Cottus asper, 52 - 100 mm), California roach (Hesperoleucus

symmetricus, 54 - 82 mm), and three-spined stickleback (Gasterosteus aculeatus, 34 - 50 mm)

were collected. Like the target species, these are all invertivores previously employed as Hg

biosentinels in California [14, 15, 45-47].

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Sample preparation and analysisAll fish collection and preparation followed protocols developed at UC Davis, with slow

cooling euthanasia method certified by the UC Davis Veterinary School's Institutional Animal

Care and Use Committee. Fish were measured for total length, rinsed with site water, and sorted

into labeled, freezer-grade plastic bags as composites for analysis, field frozen with air excluded

and water surrounding, on dry ice, and subsequently transferred to a -20 C laboratory freezer.

Composite whole body fish samples were subsequently thawed, weighed, dried to constant

weight at 55 C, dry weight and percent solids recorded, and ground to a fine homogenous

powder. Samples were analyzed for total Hg at the University of California-Davis. Analysis

employed standard cold vapor atomic absorption (CVAA) spectrophotometry, using a dedicated

Perkin Elmer Flow Injection Hg System (FIMS) with an AS-90 autosampler, following a 2 stage

digestion at 90 C in a mixture of concentrated nitric and sulfuric acids with potassium

permanganate. Routine analytical QA/QC included 20 QA/QC samples for every 30 analytical

samples, and included blanks, aqueous standards, continuing control standards, standard

reference materials with certified levels of Hg, laboratory split samples, matrix spike samples,

and matrix spike duplicates. All results met QA protocols of the Regional Monitoring Program

for Water Quality in San Francisco Bay and were well within laboratory control limits. All study

Hg results are reported on a wet weight basis.

Geospatial dataGeospatial data were developed in ArcGIS v10. The Bay shoreline was partitioned into

open water versus embayment site categories based on visual inspection of a Bay shoreline

vector file with depth data overlay, and satellite imagery. Inclusion criteria were depth, degree of

separation from the rest of the Bay, and presence of channels or sloughs. The embayment layer

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included habitats throughout the Bay, with the largest areal coverage north of San Pablo and

Suisun Bays (Supplemental Data, Figure S2).

Two numeric geospatial attributes were examined for association with fish Hg: percent

surrounding wetland area and distance from the Guadalupe River. Percent surrounding wetland

area was based on a 500 m buffer, using data from Bay Area Aquatic Resource Inventory and

Association of Bay Area Governments 2005 land-use polygons. Percent surrounding wetland

was defined as the sum of the depressional, marsh, and tidal ditch land cover categories. Distance

from the Guadalupe River, defined as the nautical distance from the westernmost tidal point of

Coyote Creek, was negatively correlated with forage fish Hg at 22 sites sampled previously [13].

It was calculated following along the deep Bay channel, extending from the starting point to the

upstream study extent of Suisun Bay (Mallard Island, near the confluence of the Sacramento and

San Joaquin Rivers). Distance from the Guadalupe River indicates how close the sites are to the

Hg contaminated New Almaden Mining District, which drains into the Lower South Bay near

the community of Alviso. However, distance from the Guadalupe River also indicates general

position along the Bay axis, with the most distant north Bay segments (Suisun Bay, San Pablo

Bay) having potentially different net MeHg production and distribution from the progressively

closer Central Bay, South Bay, and Lower South Bay [13, 26].

Data analysis

Data analyses were performed using the linear mixed effects model function in R, version

2.15 [48]. Hg data were log10 transformed to improve residual normality and variance

homoskedasticity. Topsmelt and Mississippi silverside were analyzed separately. In line with the

study questions, 4 separate linear models were built to examine the potential effect of spatial

trend (distance from Guadalupe River); embayment category (embayment versus open Bay);

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surrounding wetland abundance; or site type (i.e., POTW, contaminated sediment, industrial

watershed, and random sites) on fish Hg. Model evaluation was performed manually, using

backwards elimination of non-significant model terms. Parameter inclusion was based on the

likelihood ratio test (with an alpha = 0.05 to retain a parameter) in combination with information

theoretic criteria (i.e., AIC and BIC) [49]. Random effects were included to account for

variability among sampling sites [50]. When significant, the slope for fish length was also

allowed to vary by site. Four samples (3 Mississippi silverside and 1 topsmelt) were removed

from the statistical analyses because their inclusion would have violated assumptions of residual

normality and variance homoskedasticity. However, when analyses were performed with these

samples included, the results were essentially unchanged. More details on the modeling approach

and outlier removal are provided in the Supplemental Data Text.

Of the 4 mine sites, Mississippi silversides were only present at the Guadalupe River

upstream of Alviso Slough and topsmelt were only present at American Canyon Creek, draining

Borges Mine. Since this was insufficient to statistically evaluate a mine site effect for these

species, each mine site was compared to other data reported for additional species on an ad hoc

basis. To provide context, data on additional species were compared to previously published Hg

concentration data from mine sites [14, 46, 47] and unpublished data from reference (i.e., no

known mine influence) sites. Unpublished data were obtained via queries performed on March

23, 2013 of the California Environmental Data Exchange Network(www.ceden.us), a

collaboratively developed statewide environmental water quality database [51].

RESULTS

Graphical analysis indicated a spatial trend in average forage fish Hg concentrations, with

the highest concentrations in and adjacent to Lower South Bay, and concentrations progressively

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decreasing towards South, Central, San Pablo, and Suisun Bays (Figure 1, Figure 2). This spatial

gradient was more pronounced for Mississippi silverside (Figure 1), whereas topsmelt exhibited

more local scale spatial heterogeneity, particularly within Central Bay (Figure 2).

Hg concentrations were higher in Mississippi silversides (0.090 0.058 g/g, mean

SD,N= 237) than topsmelt (0.041 0.015,N= 239), as reported in a prior study [13]. Total

length was positively related to Hg and therefore included as a covariate in all models. Sampling

year differences (treated as a categorical variable) were significant and included in some models

(Table 1). Mixed models were needed to account for correlations among samples within a site,

with site treated as a random effect. Additionally, a significant effect of site on the length

covariate was observed for some models, and was thus incorporated as a random site effect on

the length vs. Hg slope (Table 1).

Distance from Guadalupe River

Distance from the Guadalupe River (Question 1) was negatively related to Hg in

Mississippi silverside (r= -0.69,N= 237, Figure 1) and topsmelt (r= - 0.42,N= 239, Figure 2).

Distance was also a significant predictor in mixed models accounting for site effect (p < 0.0005,

Table 1), and was therefore included as a covariate in models testing for other effects. The

distance effect varied among sampling years. For silverside, in 2009, the decrease in Hg with

distance from the Guadalupe River was weaker than other years (DistanceGuadalupe*Year2009

interaction, Figure 3). Based on model predicted concentrations, in 2009, the closest site to the

Guadalupe River (Coyote Creek upstream of Alviso Slough) exhibited two-fold higher Hg

concentrations than the furthest site (Kirker Creek near Pittsburg; 0.11 vs. 0.053 g/g), whereas

in 2010, the predicted difference was four-fold (0.16 vs. 0.039 g/g). For topsmelt, in 2008, the

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overall Hg decrease with distance from the Guadalupe River was weaker, compared to other

years (Year2008*DistanceGuadalupe).

Embayment and fringing wetland effects

Hg concentrations in Mississippi silversides collected in embayment sites were not

significantly different from Hg in Mississippi silversides collected in open water sites (Question

2; likelihood ratio testp = 0.096; Supplemental Data, Table S2). However, for topsmelt, Hg

concentrations were significantly elevated in embayment sites compared to open water sites (p =

0.012), and embayment site Hg significantly increased with distance from the Guadalupe River

and with fish length (Table 1, Supplemental Data, Table S3). Embayment sites in Central and

San Pablo Bays were more often elevated in topsmelt Hg versus adjacent open water sites

(Figure 2, Figure 4). For example, at the embayment site furthest from the Guadalupe River (the

Petaluma River site), model predicted topsmelt Hg would be 0.043 g/g, whereas an open site at

the same distance would have a predicted Hg of 0.029 g/g.

Percent surrounding wetlands (Question 3) was not a significant predictor of Hg for

Mississippi silverside or topsmelt. For both species, the final model included a significant

increase with body length, a significant decrease with distance from the Guadalupe River, and no

effect of wetlands (Table 1, Supplemental Data, Tables S4 and S5). For Mississippi silverside,

the highest mercury wetland sites were in channels surrounding San Pablo and Suisun Bays, and

had lower Hg than Lower South Bay and South Bay sites (Figure 1).

Source site type effects

Source site effects (Question 4) varied between Mississippi silverside and topsmelt. In

2008, Mississippi silverside Hg was lower at POTW sites than other site types

(SourcePOTW*Year2008 interaction, Figure 3, Supplemental Data, Table S6). Based on model

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predictions for average length fish, in 2008, POTW sites had approximately one-half of the Hg

of non-POTW sites (0.035 vs. 0.068 g/g); in 2009 and 2010, POTW sites were predicted to be

0.015 g/g lower than non-POTW sites. Graphical analysis indicated POTW sites to be lower

than nearby sites in both 2008 and 2010 (Figure 3). In 2009, there was no apparent pattern of

POTW versus other sites. Topsmelt were only obtained at 1 POTW site, the Hayward wastewater

treatment plant discharge pond, monitored in 2010. Topsmelt Hg concentrations at that site

(0.021 0.0005 g/g,N= 4) were less than half the concentrations at the nearest site measured

in 2010, the Eden Landing Shoreline (0.045 0.007 g/g,N= 4).

Hg in topsmelt was moderately elevated at contaminated sediment sites (p = 0.032, Table

1, Supplemental Data, Table S7), which were only present in Lower South, South, and Central

Bays (Figure 5). The model predicted topsmelt Hg at a contaminated sediment site to be 1.2

times that predicted for another site type in the same location.

Fish species captured varied across the mining sites (Table 2), likely due to variable

salinity conditions. The Guadalupe River upstream of Alviso Slough, which drains from the New

Almaden Mine watershed, was elevated in Mississippi silverside Hg, consistent with the general

spatial gradient observed in the present study and elsewhere [3, 13, 21, 25]. Concentrations at

this site were within the range of spatial variation observed in Lower South Bay (Figure 1), but

higher than the Baywide average and Mississippi silversides from Hg contaminated Clear Lake

[14]. The Guadalupe River site also had extremely high Hg in three-spined stickleback. In the

Napa River below the Bella Oaks Mine watershed, prickly sculpin Hg was comparable to Clear

Lake [14] and higher than the average of 8 sites from the Sacramento-San Joaquin Rivers Delta.

Napa River California roach Hg was higher than the average of 8 CA statewide sites lacking

mine influence, but well below the concentration previously measured by Slotton et al. [46] at

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Marsh Creek, a mine dominated creek that drains into Suisun Bay. American Canyon Creek,

which drains from the Borges mine, was not elevated in topsmelt Hg, relative to general

Baywide concentrations. Dry Creek also had relatively low Hg concentrations in prickly sculpin

and California roach, and unremarkable concentrations in three-spined stickleback, suggesting a

lack of influence of the nearby La Joya mine.

Three-spined stickleback were relatively low in Hg within the urbanized industrial

watershed of Zone 4 Line A, compared to mine sites and 4 other Bay sites. The Zone 4 Line A

sampling location is within a flood drainage channel, several km above the Bay shoreline [52].

DISCUSSION

We found that forage fish Hg concentrations were elevated in the southern Bay. This

pattern has been noted previously [13], as well as elevated Hg or MeHg in southern Bay water,

sediment, and shorebirds [3, 26, 53], suggesting that greater attention be dedicated to MeHg

management in this region. The association between Hg and distance to the Guadalupe River

indicates that Hg bioaccumulation in San Francisco Bay exhibits a spatial gradient across the

relatively large distance of approximately 146 km from Coyote Creek upstream of Lower South

Bay to the east side of Suisun Bay downstream of the Sacramento-San Joaquin Rivers Delta. A

spatial gradient is also apparent in 202Hg stable isotope along the Bay for sediment and forage

fish, suggesting increased bioaccumulation from Hg sources from the New Almaden Mining

District, draining into Lower South Bay [21, 25]. The presence of tidal mixing and fluvial

transport over time may create a relatively smooth gradient of both Hg source material and

MeHg biogeochemistry. Results from the present and previous studies suggest that in the western

United States, fish Hg bioaccumulation exhibits regional spatial gradients, often following

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gradients of Hg mass in the sediments due to proximity to mines and other legacy Hg sources [5,

11, 14, 54, 55].

The higher Hg concentrations in Lower South Bay and South Bay likely result from

multiple factors including historical Hg loading from the New Almaden Hg Mining District,

South Bay hydrodynamics, and methylation in the Bay and adjacent habitats. Relatively long

water residence times in Lower South Bay and South Bay may result in reducing conditions that

favor sediment and water column MeHg production [3], with additional elevated MeHg

production in the extensive salt pond complexes adjacent to Lower South Bay [31, 32], and

periodic anoxia along Alviso Slough itself[16].

Elevated Hg in topsmelt but not Mississippi silverside at embayment sites (e.g., marinas,

creeks, and backwater sloughs), and no relationship between surrounding wetlands and fish Hg,

suggest a limited ability to predict biotic MeHg exposure based on natural landscape attributes.

We hypothesized that surrounding wetland abundance would correlate with forage fish Hg based

on the established role of freshwater wetlands as MeHg sources to adjacent waters [34], the

consequent association between proximity to wetlands and freshwater fish Hg [12, 18, 35, 36],

and evidence of elevated MeHg production in estuarine wetland sediment [30, 33, 56]. However,

for these forage fish that reside within the subtidal open waters of the Bay, MeHg concentrations

were decoupled from fringing wetland abundance. This is in contrast to northern temperate lakes,

which are dominated by atmospheric deposition, and frequently exhibit at least a moderate effect

of catchment wetland abundance and other landscape attributes on MeHg bioaccumulation [12,

18, 34, 57]. This finding suggests that the extensive wetland restoration activities planned for

San Francisco Bay are not likely to adversely affect MeHg exposure for these subtidal Bay

forage fish or their predators. Nevertheless, the Bay and associated wetlands comprise a range of

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habitats, and changes in Hg exposure to organisms residing within the wetlands or ponds

fringing the Bay could still occur as a result of restoration or other management activities [32].

Our hypothesis that embayment status could predict increased MeHg exposure in forage

fish was based on elevated Hg accumulation in Bay forage fish species that heavily utilize

intertidal and shoreline areas (e.g., Mississippi silverside) [13], elevated sediment and biota

MeHg in proximity to freshwaters in the Bay and other estuaries [26, 37-40], increased exposure

to anthropogenic Hg pollution at embayment sites [4, 31], and the possible importance of

fringing wetlands, intertidal mudflat habitat, and shallow sediments for MeHg production at

embayment sites [30, 38, 56]. The increase in topsmelt Hg from embayment sites was related to

spatial location; differences were primarily observed in Central Bay, where Mississippi

silversides were not readily available. We speculate that the embayment pattern for topsmelt

largely stems from exposure to historic industrial contamination, because topsmelt Hg was also

increased near legacy contaminated sediment. Historic industrial activity was abundant along the

Central Bay shoreline, and is associated with elevated concentrations of PCBs, another legacy

and industrial pollutant, in sediment and forage fish [58, 59]. This pattern suggests that regional

priorities for minimizing MeHg production might focus on identifying and restoring those

embayment sites with elevated sediment and biota MeHg.

Source site type effects included higher topsmelt Hg near contaminated sediments, higher

Hg near some historic mine drainages, and lower Hg adjacent to POTWs in 2008 and possibly

2010. Previous research suggests that Bay forage fish Hg and PCBs are sediment derived[25,

59], and we observed that topsmelt but not Mississippi silverside Hg corresponded to

contaminated sediment sites. Other studies have also exhibited variable relationships between

fish and sediment Hg (or MeHg), with associations observed in Texas rivers [11], the Hudson

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River (New York/New Jersey) [60], and the Willamette River (Oregon/Washington) [5], but not

in a survey of northeastern US freshwaters [57] or a Columbia River (Washington) reservoir

[61]. In the Gulf of Maine, biota Hg is generally elevated in regions with elevated sediment Hg,

but the bioaccumulation factor is lower in more contaminated areas, due to elevated total organic

carbon reducing bioavailability [43]. The complexity of Hg methylation and bioavailability,

biota movement, and food web structure all contribute to the weak and variable relationships

between fish and sediment Hg [43, 61, 62].

The negative effect of POTWs on forage fish Hg was unexpected given that average total

MeHg detected in discharge water from the 16 largest Bay POTWs was 0.37 ng/L, versus 0.096

ng/L in Bay ambient water[20]. We speculate that lower than expected forage fish Hg

concentrations at some POTW sites may result from biodilution, in which increased primary and

secondary production decreases Hg bioaccumulation and biomagnification [63, 64]. The reduced

Mississippi silverside Hg concentration at 4 South Bay POTW sites is associated with elevated

discharge water ammonium concentrations, compared to ambient Bay conditions [65]. This may

result in increased rates of primary production, higher densities of Mississippi silversides and

their invertebrate prey, or more rapid growth rates, all resulting in decreased tissue Hg

concentrations. Forage fish densities during collections at these sites were also observed to be

substantially greater than typical for the Bay (D.G. Slotton, personal observation).

We observed inconsistent impacts of local mining, especially compared to the broad

spatial gradient across the Bay. Concentrations in proximity to mining-impacted sites varied

widely: the Guadalupe River downstream of New Almaden Mining District and the Napa River

below the Bella Oaks Mine were elevated in fish Hg, and at or above prior measurements of the

same fish species in mine influenced sites [14, 46]. In contrast, American Canyon Creek and Dry

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Creek were not elevated, suggesting lower levels of residual contamination. In California roach

monitored closer to the New Almaden Mines (Guadalupe Creek at Meridian Ave and Alamitos

Creek at Harry Road), Hg concentrations were even greater, versus other sites in the local

Guadalupe River watershed[66], and Hg isotopes indicate a New Almaden mining source signal

in sediment and forage fish [21, 25]. In freshwater lakes and rivers, fish Hg concentrations are

frequently elevated in sites impacted by mining waste versus reference sites, and tend to decrease

with increasing distance from mining sources [5, 14, 55, 67, 68]. Hg is elevated near mines,

processing facilities, or waste tailings even in areas with naturally occurring Hg deposits, and

even with Hg mining completed several decades before fish collection. This indicates a

remaining concern for mine Hg in the food web and a potential benefit of ongoing remediation

focused on Hg mining sources such as the New Almaden Mining District [3].

Finally, sites adjacent to industrial watersheds hypothesized to be Hg-contaminated did

not exhibit elevated forage fish Hg concentrations. This is consistent with the relatively small Hg

mass discharged from these industrial watersheds, compared to other sources and Bay sediment.

The San Francisco Bay TMDL Staff Report [22] estimates urban stormwater runoff to contribute

92 kg/yr Hg to the Bay, which is only 7.5% of all sources (1222 kg/yr) [22], and Hg isotope

studies found a significant relationship between sediments and forage fish, without any notable

deviations adjacent to more industrial sites [25]. Even stickleback collected within a small

industrial watershed (Zone 4 Line A) were lower than at other sites, suggesting that industrial

watersheds are not locations of elevated MeHg bioaccumulation.

We demonstrated the use of biosentinel forage fish, combined with a stratified

probabilistic survey design, to identify Hg bioaccumulation spatial patterns and sources in a large

urbanized estuary. Both regional and local patterns were observed, reflecting the complex legacy

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Hg sources and system hydrology. Regionally, there was a clear spatial gradient with distance

from a historic Hg mining district. After accounting for that gradient, local differences among

sites were subtle and varied between fish species. These findings suggest that forage fish Hg

bioaccumulation predominantly exhibits broad regional variation, and that sources varying at

local scales, including POTWs and legacy sediment Hg contamination, exhibit a secondary

influence.

SUPPLEMENTAL DATA

Forage fish mercury spatial patterns and predictors in San Francisco Bay (Supplemental

Text, Tables and Figures), and field and laboratory Hg data on 1260 forage fish samples

(SFForageFishHg.csv).

ACKNOWLEDGMENT

N. Feger, C. Sommers, R. Looker, R. Schlipf, and the RMP Technical Review

Committee assisted with site selection. S.M. Ayers, K. Ridolfi, A.R. Melwani, R.M. Allen, and

M.A. Lent assisted with field sampling. A.R. Melwani and J. Griswold helped with statistical

analysis, and R.M. Allen and M. Klatt helped with data interpretation. J.A. Davis, D.B. Senn,

M.D. Sedlak, M. Lahiff, and two anonymous reviewers constructively reviewed drafts of the

manuscript. Site access was provided by CDPR, CDFG, East Bay RPD, Mt. View Sanitary

District, USACE, and SF Bay National Wildlife Refuge. The Regional Monitoring Program for

Water Quality in San Francisco Bay funded the study (SFEI Publication 694), with additional

support by a USEPA STAR Fellowship to B.G.

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use of pre-breeding American avocets and black-necked stilts in San Francisco Bay. Sci Total

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in contaminated pelagic and wetland sediments of San Pablo Bay, California.Environ Geol

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Franklin D. Roosevelt Lake and the Upper Columbia River, Washington. T Am Fish Soc

126:477-487.

62. Fowlie AR, Hodson PV, Hickey MBC. 2008. Spatial and seasonal patterns of mercury

concentrations in fish from the St. Lawrence River at Cornwall, Ontario: Implications for

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Greenfield BK, Buckman KL, Lamborg CH. 2012. Nutrient supply and mercury dynamics in

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Memorandum 5.3.2. Data Collection Report. Prepared for Santa Clara Valley Water District,

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Lake Region, British Columbia, Canada.Environ Pollut131:275-286.

68. Leady BS, Gottgens JF. 2001. Mercury accumulation in sediment cores and along food

chains in two regions of the Brazilian Pantanal. Wetl Ecol Manag 9:349-361.

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Table 1.Results of study model evaluationsFinal model

Test (Questions) a Species N Likelihood

ratio

p value Fixed terms (Effect sign) Random

terms

Distance from Guadalupe b (1) Silverside 237 44.8 0.072

cific

cean

C

a

l

i

f

o

r

n

ia

SouthBay

Suisun

Bay

Lower

South

Bay

Topsmelt

Hg (g/g)


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qqqq

qqqq

qqqq

q

qqqq

qqqq

q qqq

qqq

qqq

qqq

qq

qqqq

qqqq

q

0 50 100

0.02

0.05

0.20

2008

qPOTWOther

qqq

qq

qqqqq

qq q

qqq

qq

qqq

q

qq

q

qqq

q

q

q

q

qqq

qq

qqq

qqqq

qqqq qq

q

qqq

q

0 50 100

0.02

0.05

0.20

2009

qPOTWOther

qq

qqq

qqq

qqqq q

qq

q

qqq

qqq q

qq

qqq

q

qq

q

qqqq

q

q

q

q

q

q

qqq

qq

qqqq

qqq qqq

0 50 100

0.02

0.05

0.20

2010

Distance from Guadalupe River (km)

qPOTWOther


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q

qqq

qq

qq

qq

q

qq

q

qq

q

q

q

q

qq

q

qq

q

qq

q

qqqq

qq

q

qq

q

q

qq

0 20 40 60 80 100 120

0.0

2

0.03

0.0

4

0

.06


y(gg

)

qOpen

Embayment


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q

qqq

qq

qq

qq

q

qq

q

qqq

q

q

q

qq

q

qq

q

qq

q

qqqqq

q

q

qq

qqqqqq

q

qqqqqq

q

q

qq

q

q

q

q

qq

qqq

q

q

qq

qq

q

q

qq

q

q

qq

q

qq

q

qqq

q

qq

q

qq

qq

qqq

q

qqq

qqq

q

qq

q

qq

qq

qq

qqq

q

q

qq

q

qqq

q

qq

qqq

q

qq

q

qq

qqq

qq

qq

0 20 40 60 80 100 120

0.02

0.0

4

0.0

6

0.1

0


y(gg

)

qContaminated sediment

Other


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Supporting document for

Predictors of mercury spatial patterns in San Francisco Bay forage fish

Corresponding author:

Ben K. GreenfieldEnvironmental Health Sciences DivisionSchool of Public HealthUniversity of California-Berkeley, 50 University Hall #7360Berkeley, CA 94720-7360Tel: 1 510 507 2365E-mail:[email protected]

14 pages total

Section I: Supplemental Text. p. 2Study hypothesesStudy parametersSite selection descriptionData analysis methodsRemoval of outliers

Section II: Supplemental Tables. p. 5Section III: Supplemental Figures. p. 8Section IV: Description of Supplemental Data. p. 10Section V: References. p. 13

1
mailto:[email protected]:[email protected]:[email protected]:[email protected]


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Section I: Supplemental Text

Study hypotheses

The study design and site selection were intended to answer the 4 questions listed in theIntroduction. Based on prior Bay studies [1-5], input from local natural resource managers, andcurrent conceptual models regarding MeHg cycling and bioaccumulation in estuaries, wedeveloped the following 4 hypotheses regarding factors that influence small fish Hgconcentrations:

1. Mercury concentrations will increase with proximity to the Guadalupe River, in theLower South Bay.

2. Concentrations will be higher in fully or partially enclosed areas, defined to includenatural or man-made coves or channels, or estuarine creeks draining into the Bay (defined in thispaper as embayments). These areas would tend to have low hydraulic mixing of subtidal water(i.e., locations with low water turnover rate), resulting in higher MeHg production.

3. Concentrations will be positively correlated with nearby wetland abundance.4. Concentrations will be higher near mercury source areas, including urban or industrial

watershed drainages, wastewater treatment plants (i.e., publicly operated treatment works, orPOTWs), areas with historically Hg or MeHg contaminated sediments, and mine drainages.

Study parametersAverage total body length (mm) was based on field measurements of all individuals in a

composite sample. Length is a widely reported correlate of fish Hg, and length correction isneeded[6, 7], including for small fish evaluated in the Bay [2, 8]. Sampling was performed in 3years: 2008, 2009, and 2010, which are treated as categorical variables (with 2010 as the basecondition). There are also 4 categorical variables indicating different kinds of Hg source sites

(Table S1), as well as randomly chosen sites that represent background conditions (statisticallytreated as the base condition).

Site selection descriptionCreeks draining Hg mines (N= 4) were chosen based on the priority scheme of Abu-Saba

[9]. Sites were included based on connectivity to the Bay, evidence of mine waste discharginginto State waters, and risk to fishery resources or other sensitive habitat areas. Three creeks werechosen based on drainage from mines meeting the inclusion criteria: Napa River (drainage fromLa Joya and Bella Oaks mines), American Canyon Creek (Borges Mine), and Guadalupe River(New Almaden Mining District). Due to the small number of candidate sites, all Hg minedrainage sites were sampled. To further evaluate the potential mine signal from La Joya mine, a

freshwater site adjacent to and draining the mine (Dry Creek) was added and sampled in 2009.POTW sites (N= 7 sites) were selected from among those Bay POTWs that are identified by

the San Francisco Bay Regional Water Quality Control Board (Regional Board) as shallow-waterdischarge POTWs [10]. The selection of shallow water discharges was based on the expectationof greater potential impact of POTW discharge to the nearshore area biogeochemistry inshallow-water environments than deep-water or offshore environments. That is, shallow-waterPOTW sites had a relatively high water volume ratio of discharge water to natural Bay water,potentially resulting in discharge water impacting Hg biogeochemistry. The original pool of

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sites was further reduced to only include sites having summer discharge because samplingoccurred in the fall. The final POTW sites were City of American Canyon Wastewater TreatmentPlant, Fairfield-Suisun, Hayward Pond 3B, Mountain View Sanitary District Peyton Slough, Cityof Palo Alto, City of Sunnyvale, and Sonoma Valley County Sanitary District Schell Creek. All 7POTW sites were sampled.

Candidate sites with relatively elevated sediment total Hg or MeHg (N= 35) were selectedbased on 2 prior sediment surveys from the Bay Protection and Toxic Cleanup Program [11] anda study funded by the Regional Board and the California Bay-Delta Authority program [3]. Bothstudies targeted areas known to be currently or historically industrial or otherwise suspected ofhaving high contamination. Sites were included when sediment THg concentrations were greaterthan 700 ng g-1 or MeHg concentrations were greater than 2 ng g-1. In the GRTS sample draw, 15sites were sampled from this category.

Candidate sites draining industrial and urban watersheds (N= 21) were selected based on acombination of 4 attributes in the watersheds: the documented presence of historic mercuryspills, density of historic industrial sites, density of railway lines, and density of car recyclers.Toxic Hg spills were identified using database queries from the CA Department of Toxic

Substances Control, USEPA Superfund, and Toxic Release Inventory. Railway line density wasconsidered as an indicator of historic industry, while auto recycler density indicated currentindustry and potentially an additional Hg source. All attributes were characterized using GISlayers developed from Lower South Bay to southern San Pablo Bay [12]. To increasegeographical coverage, 3 sites were added from central San Pablo Bay and Suisun Bay (KirkerCreek, Corte Madera Creek, and Alhambra Creek). In the GRTS sample draw, 13 sites weresampled from this category.

In 2008, 12 sites adjacent to fringing wetlands were sampled to aid in evaluating the potentialimpact of wetland proximity on biosentinel Hg (Hypothesis 4). The wetland sites ranged inanticipated frequency of wetting and drying; wetlands with a high expected wetting and dryingfrequency were hypothesized to exhibit higher MeHg production and consequently higher Hg in

biosentinels [13]. Results from 2008 indicated no apparent correspondence with fringing wetlandabundance or type, and GIS indicated that a range of proximity to wetlands was achieved usingthe random samples in the GRTS design. Therefore, in 2009 and 2010 wetland site targeting wasdiscontinued to increase sample sizes in the other strata. The final study analysis compared fishHg based on percent wetlands at the site. The wetland sites were included in analysis ofproximity to wetlands vs. small fish Hg (Question 3). To avoid confounding site categorization,the 2008 wetland sites were excluded from the comparison of embayment versus open sites(Question 2) and the comparison of random versus source sites (Question 4).

Data analysis methodsWe employed the 10 step approach to nested data recommended by Zurr et al. [14] (Sections

4.2.3 and 5.10), to assess the need for mixed models. In all cases, model fit and residualbehavior significantly improved when including a random term for sampling site. Therefore, allmodels included a random intercept effect for site, and a random slope (i.e., length) effect for siteif warranted. The initial model fixed structure always included year terms (2008 and 2009), fishlength, distance from the Guadalupe River, and the effect under consideration (embaymentcategory, site type, or surrounding wetland), and one way interaction terms between site effectsand the other model terms. For example, the initial model to evaluate embayment effect was:Log(Hg) = Year2008 + Year2009 + FishLength + DistanceGuadalupe + Embayment +

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Year2008*Embayment + Year2009*Embayment + FishLength*Embayment +DistanceGuadalupe*Embayment.

The embayment category statistical evaluation (Question 2) was performed on random sitesonly, to avoid confounding site type versus embayment category. The silverside site typeevaluation (Question 4) compared contaminated sediment, industrial watershed sites, POTW,

and random (open and embayment) sites. The topsmelt site type evaluation did not includePOTW sites because topsmelt were only collected at 1 POTW site.

Removal of outliersFour outlier samples were removed from statistical analysis because their inclusion

would have violated linear model assumptions. For silversides, the Cooley Landing site (N= 3samples, located west of Lower South Bay) had extreme variance heterogeneity due to onlyhaving 1 individual per sample, which caused violation of normality in residuals. For topsmelt, 1of the composite samples collected in Alviso Slough (south of Lower South Bay) in 2009 was anoutlier (standardized residual = 4.68), with an Hg concentration of 0.235 g/g, versus a range of0.015 to 0.114 g/g for the remaining 239 topsmelt samples. Other than Figure 1, all results are

reported excluding these outlier samples. However, when the analysis was performed includingthese samples, results (statistical significance and effect size and direction) were unchanged.

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Section II: Supplemental Tables

Table S1. Parameters examined in study.ID in Models Description Type Units

Hg Hg concentration in composite fish sample, wet

weight. Obtained from single species compositesamples, log10 transformed for model inclusion

Numeric g g-1

TLengthCen Fish total body length, averaged across compositesample, centered before model inclusion

Numeric mm

Station Site Location ID.N= 99 stations; but only a subsetfor each species and analysis.

Categoricala

DistGuadCen Distance from Guadalupe River of collection site,centered before model inclusion

Numeric km

Y2008 Indicates samples collected in 2008 Categorical 1=YesY2009 Indicates samples collected in 2009. Default (i.e.,

baseline) year is 2010Categorical 1=Yes

WetlandAbund Surrounding wetland area, based on a 500 m buffer Numeric %Embayment Indicates sample collected from enclosed

embayment, rather than open Bay shoreline (FigureS1)

Categorical 1=Yes

SourcePOTW Publicly operated treatment works (POTW) atstation. This is influenced by wastewater treatmentplant discharge. This and remaining source stationcategories are compared to randomly selectedstations.

Categorical 1=Yes

SourceContamSed Historic Hg contaminated sediment at station Categorical 1=YesSourceWatershed Station adjacent to industrial or urban watershed

hypothesized to be high in Hg

Categorical 1=Yes

SourceMine Station adjacent to watershed containing historic Hgmine

Categorical 1=Yes

a. All categorical variables are nominal, rather than ordinal

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Model structures

Table S2. Silverside final model for embayment effects (N= 116). For this and remaining tables,likelihood ratio test is performed, and the difference in AIC (AIC) is determined, between a

model containing all parameters listed and a model with the current parameter removed. NA:

since embayment was not significant, it is not included in the final model.Fixed effects Value SE Likelihood ratio p value AIC

(Intercept) -1.20219 0.01802

TLengthCen 0.00516 0.00190 39.5


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Table S5. Topsmelt final model for wetland effects (N= 269). NA = wetland was not significant,and was therefore not included in the final model.Fixed effects Value SE Likelihood

ratio

p value AIC

(Intercept) -1.39659 0.01656TLengthCen 0.00379 0.00051 38.7


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Section III: Supplemental Figures

Figure S1. Study sample locations.

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Figure S2. Final stratification of the Bay shoreline for the random sample draw. The red linerepresents the embayment stratum. Blue areas not parallel to a red line represent the openstratum.

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Section IV: Description of Supplemental Data File

All forage fish Hg data collected in San Francisco Bay from 2008 to 2011 are provided as acomma separated (CSV) file (filename: SFForageFishHg.csv). Comprising 1260 compositesamples, these data are more extensive than the samples analyzed for the present study. They

include Bay forage fish Hg data analyzed for temporal patterns and published elsewhere [8], aswell as samples collected and analyzed for Hg but falling outside the scope of both studies. Dataon fish Hg and other contaminants are also presently available via the California EnvironmentalData Exchange Network(www.ceden.us)[15]

This file contains 30 data fields, including Hg concentrations, site and sample descriptiveinformation, and ancillary information. Each row corresponds to a separate composite fishsample analyzed for Hg:

Sample ID Laboratory identifier indicating the composite fish sample analyzed

Site ID Unique identifier for each collection site

Collection CodeUnique identifier for each collection event (i.e., each site and sample datecombination)

Site DescriptionDescriptive name for each collection site

Site TypeIndicates the site category each sample was included in. Table S8 (below) lists allpossible categories

Date Collection date

LatitudeIn degrees and decimal degrees

Longitude In degrees and decimal degrees

Species Common name of the sampled species. Table S9 lists corresponding scientific names, aswell as number of samples collected per species

HgDw Mercury concentration (g g-1 dry weight)

Moisture Tissue proportion moisture

HgWw Mercury concentration (g g-1 wet weight)

NNumber of individuals in the composite sample

Total Length Average total length of individuals in the composite sample (mm)

Distance Guadalupe Distance from the Guadalupe River, following along the deep Bay channel

(further described in Methods)WetlandAbund Percent surrounding wetland area within a 500 m buffer of collection location

The remaining variables are binary categorical variables (1 = yes; 0 = no), indicating whichstudy model evaluation (Table 1) or sampling strata a sample was included in.

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Question1SpatialTrend Sample included in study Question 1: What are the spatial trends inforage fish Hg?

Question2Embayment Sample included in study Question 2: Are Hg concentrations elevated inembayments relative to open water sites?

Question3WetlandsSample included in study Question 3: Does extent of fringing wetlandhabitat correlate with Hg concentrations?

Question4SiteType Sample included in study Question 4: Are Hg concentrations elevated atpotential source sites, relative to randomly selected sites?

LongTerm Sample included in prior analysis of long term Hg trends [8]

Source Sample is in 1 of the 4 source site categories

Random Sample is in the random strata (either embayment or open) sampled from entire Bayshoreline

SourcePOTW Wastewater treatment plant source site sample

SourceMine Historic Hg mine source site sample

SourceContamSed Hg or MeHg contaminated sediment source site sample

SourceWatershed Urban or industrialized watershed source site sample

Embayment Site falls within the embayment stratum (1 = embayment; 0 = open; Figure S2)

OffSeason Sample collected outside the Fall season sampling window required for studyinclusion. The study sampling window was August 27 to November 30

Wetlands Sample targeted to increase wetland coverage

Table S8. Site type descriptions.Site type a Description

Embayment Random Bay shoreline site; embayment stratum (Figure S2)Open Water Random Bay shoreline site; open water stratum (Figure S2)Source ContaminatedSediment Source site with elevated sediment THg or MeHgSource Wastewater TreatmentPlant (POTW) Source site draining wastewater treatment plantSource Industrial Watershed Source site draining urban and industrial watershedSource Hg Mine Source site draining historic Hg mine watershedWetlands Site adjacent to nearshore wetland, targeted to increase

wetland coverage, sampled in 2008Long Term Monitoring Site monitored for annual variation from 2005 to 2010,

analyzed elsewhere [8]Seasonal/Long TermMonitoring

Site monitored for seasonal and annual variation, analyzedelsewhere [8]

Not in Hg Sampling Design Site targeted for PCB study [16], analyzed for Hg but notincluded in Hg study analyses

a. Some sites are in more than 1 category

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Table S9. Common and scientific names, and total number composite samples collected for eachspecies.Common Name Scientific Name Number samples

American shad Alosa sapidissima 7Arrow goby Clevelandia ios 105

California roach Hesperoleucus symmetricus 8Diamond turbot Hypsopsetta guttulata 6Golden shiner Notemigonus crysoleucas 3Longjaw mudsucker Gillichthys mirabilis 1Mississippi silverside Menidia audens 357Northern anchovy Engraulis mordax 24Prickly sculpin Cottus asper 8Rainwater killifish Lucania parva 27Shimofuri goby Tridentiger bifasciatus 3Shiner perch Cymatogaster aggregata 1Staghorn sculpin Leptocottus armatus 33

Striped Bass Morone saxatilis 24Threadfin shad Dorosoma petenense 2Three-spined stickleback Gasterosteus aculeatus 24Topsmelt Atherinops affinis 610Western mosquitofish Gambusia affinis 7Yellowfin goby Acanthogobius flavimanus 10

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Section V: References

1. Conaway CH, Squire S, Mason RP, Flegal AR. 2003. Mercury speciation in the San FranciscoBay estuary.Mar Chem 80:199-225.

2. Greenfield BK, Jahn A. 2010. Mercury in San Francisco Bay forage fish.Environ Pollut

158:2716-2724.3. Heim WA, Coale KH, Stephenson M, Choe K-Y, Gill GA, Foe C. 2007. Spatial and habitat-based variations in total and methyl mercury concentrations in surficial sediments in the SanFrancisco Bay-Delta.Environ Sci Technol 41:3501-3507.

4. Marvin-DiPasquale MC, Agee JL, Bouse RM, Jaffe BE. 2003. Microbial cycling of mercuryin contaminated pelagic and wetland sediments of San Pablo Bay, California.Environ Geol43:260-267.

5. Conaway CH, Black FJ, Grieb TM, Roy S, Flegal AR. 2008. Mercury in the San FranciscoEstuary: A review.Rev Environ Contam Toxicol 194:29-54.

6. Tremblay G, Legendre P, Doyon J-F, Verdon R, Schetagne R. 1998. The use of polynomialregression analysis with indicator variables for interpretation of mercury in fish data.

Biogeochemistry 40:189-201.7. Wiener JG, Bodaly RA, Brown SS, Lucotte M, Newman MC, Porcella DB, Reash RJ, SwainEB. 2007. Monitoring and evaluating trends in methylmercury accumulation in aquatic biota.In Harris R, Krabbenhoft DP, Mason R, Murray MW, Reash R, Saltman T, eds,EcosystemResponses to Mercury Contamination: Indicators of Change. CRC Press, Pensacola, FL, pp87-122.

8. Greenfield BK, Melwani AR, Allen RM, Slotton DG, Ayers SM, Harrold KH, Ridolfi K, JahnA, Grenier JL, Sandheinrich MB. 2013. Seasonal and annual trends in forage fish mercuryconcentrations, San Francisco Bay. Sci Total Environ 444:591-601.

9. Abu-Saba K. 2003. Managing inactive mercury mine sites in the San Francisco Bay Region.Applied Marine Sciences,

Inc.http://www.bacwa.org/LinkClick.aspx?fileticket=RUiczIW5flU%3D&tabid=126&mid=57210. California Regional Water Quality Control Board San Francisco Bay Region. 2011. San

Francisco Bay Basin (Region 2) Water Quality Control Plan (Basin Plan). Web Document.Accessed October 11,2012.http://www.waterboards.ca.gov/sanfranciscobay/basin_planning.shtml. http://www.waterboards.ca.gov/sanfranciscobay/basin_planning.shtml

11. Hunt JW, Anderson BS, Phillips BM, Newman J, Tjeerdema RS, Taberski K, Wilson CJ,Stephenson M, Puckett HM, Fairey R, Oakden J. 1998. Sediment quality and biological effectsin San Francisco Bay: Bay Protection and Toxic Cleanup Program Final Technical Report.San Francisco Bay Regional Water Quality Control Board, Oakland,CA.http://www.swrcb.ca.gov/water_issues/programs/bptcp/docs/reg2report.pdf

12. SFEI. 2010. A BMP tool box for reducing polychlorinated biphenyls (PCBs) and mercury(Hg) in municipal stormwater. San Francisco Estuary Institute, Oakland,CA.http://www.sfei.org/documents/3813

13. Snodgrass JW, Jagoe CH, Bryan AL, Brant HA, Burger J. 2000. Effects of trophic status andwetland morphology, hydroperiod, and water chemistry on mercury concentrations in fish.Can J Fish Aquat Sci 57:171-180.

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http://www.bacwa.org/LinkClick.aspx?fileticket=RUiczIW5flU%3D&tabid=126&mid=572http://www.bacwa.org/LinkClick.aspx?fileticket=RUiczIW5flU%3D&tabid=126&mid=572http://www.bacwa.org/LinkClick.aspx?fileticket=RUiczIW5flU%3D&tabid=126&mid=572http://www.bacwa.org/LinkClick.aspx?fileticket=RUiczIW5flU%3D&tabid=126&mid=572http://www.waterboards.ca.gov/sanfranciscobay/basin_planning.shtmlhttp://www.waterboards.ca.gov/sanfranciscobay/basin_planning.shtmlhttp://www.waterboards.ca.gov/sanfranciscobay/basin_planning.shtmlhttp://www.waterboards.ca.gov/sanfranciscobay/basin_planning.shtmlhttp://www.waterboards.ca.gov/sanfranciscobay/basin_planning.shtmlhttp://www.waterboards.ca.gov/sanfranciscobay/basin_planning.shtmlhttp://www.swrcb.ca.gov/water_issues/programs/bptcp/docs/reg2report.pdfhttp://www.swrcb.ca.gov/water_issues/programs/bptcp/docs/reg2report.pdfhttp://www.swrcb.ca.gov/water_issues/programs/bptcp/docs/reg2report.pdfhttp://www.sfei.org/documents/3813http://www.sfei.org/documents/3813http://www.sfei.org/documents/3813http://www.sfei.org/documents/3813http://www.swrcb.ca.gov/water_issues/programs/bptcp/docs/reg2report.pdfhttp://www.waterboards.ca.gov/sanfranciscobay/basin_planning.shtmlhttp://www.waterboards.ca.gov/sanfranciscobay/basin_planning.shtmlhttp://www.waterboards.ca.gov/sanfranciscobay/basin_planning.shtmlhttp://www.bacwa.org/LinkClick.aspx?fileticket=RUiczIW5flU%3D&tabid=126&mid=572http://www.bacwa.org/LinkClick.aspx?fileticket=RUiczIW5flU%3D&tabid=126&mid=572


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14. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. 2009.Mixed Effects Models andExtensions in Ecology with R. Springer, Berlin, Germany.

15. CEDEN. 2012. California Environmental Data Exchange Network General Information. FactSheet.http://www.ceden.org/docs/ceden_intro_010912.pdf

16. Greenfield BK, Allen RM. 2013. Polychlorinated biphenyl spatial patterns in San Francisco

Bay forage fish. Chemosphere 90:1693-1703.
http://www.ceden.org/docs/ceden_intro_010912.pdfhttp://www.ceden.org/docs/ceden_intro_010912.pdfhttp://www.ceden.org/docs/ceden_intro_010912.pdfhttp://www.ceden.org/docs/ceden_intro_010912.pdf

Documents

Predictors of mercury spatial patterns in San Francisco Bay forage fish