Marine Pollution Bulletin 64 (2012) 2399–2408
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Marine Pollution Bulletin
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Recent status of total mercury and methyl mercury in the coastal waters of the northern Gulf of Mexico using oysters and sediments from NOAA’s mussel watch program ⇑ D.A. Apeti , G.G. Lauenstein, D.W. Evans
National Oceanic and Atmospheric Administration, National Centers for Coastal and Ocean Science, United States article info abstract
Keywords: The current status of mercury concentrations in the Gulf of Mexico (GOM) were assessed using the Total mercury Mussel Watch Program (MWP) contaminant monitoring data, which is based on the analysis of oyster Methyl mercury tissue and sediment samples. In both matrices, tHg and MeHg concentrations varied broadly. Significant Oysters concentration differences (p < 0.05) between the sub-regions of the eastern, central and western Gulf Sediment were observed with maximum concentrations (hotspots) found at specific sites all across the Gulf. Coastal waters Compared to the Food and Drug Administration’s action level in seafood, maximum mercury values were Gulf of Mexico low. Based on the long-term MWP data, tHg in tissues show fairly static temporal trends along the central and western Gulf coast, while strong decreasing trends were observed in the eastern Gulf. However, the presence of mercury hotspots indicates that mercury is still a concern in the GOM. The results comple- ment existing information to further the understanding of mercury distributions in the GOM. Published by Elsevier Ltd.
1. Introduction pollution in aquatic systems (USGS, 1997; EPA, 1997a; Muir et al., 2005). Mercury loading into the GOM ecosystem is exacer- Mercury is a highly toxic, non-essential heavy metal that is bated by the sub-tropical climate, with frequent thunderstorms found both naturally and as an introduced contaminant in the that flush contaminants, including mercury, from the atmosphere environment. As a result of its widespread use (e.g. batteries, chlo- (Nair et al., 2011). Selin and Jacob (2008) concluded that atmo- rine and caustic soda production) and its release through fossil fuel spheric mercury deposition rates along the Gulf of Mexico coast burning, mercury contamination has become increasingly wide- are the highest in the US. spread in the environment (Moore, 2000). A 2004 National Science In the environment, mercury is methylated through biological and Technology Council (NSTC) report estimated that mercury use processes in anaerobic conditions, mainly by sulfate and iron in the US has declined by more than 70%. However, anthropogenic reducing bacteria (Kerin et al., 2006). The methylation process activities associated with past industrial activities, coal fired elec- primarily converts inorganic mercury to mono-methyl mercury. tric turbines, and municipal and medical waste incinerators Dimethyl mercury is also produced although it is less abundant continue to emit significant amounts of mercury into the air in the environment. Methyl mercury (MeHg) is the most toxic (EPA, 1997a; Wang et al., 2003; Selin and Jacob, 2008). According and highly bioaccumulative form of mercury because of its high to the US Government Accountability Office (GAO), anthropogenic affinity for thiol groups in proteins (EPA, 1997a; Murphy et al., activities in the US emit about 115 tons of mercury, which account 2008). Hence, MeHg tends to be retained in tissues and biomagni- for nearly half of the total mercury deposited in the US yearly fies in food chains. The understanding of mercury chemical (GAO, 2005). In the GOM, in particular, mercury deposition into behavior in the environment has progressed in recent years, as ecosystems is linked to contributions from the Mississippi River increasing levels of mercury contamination have been measured transport, offshore oil and gas operation and past chlor-alkali plant in aquatic and coastal habitats around the US. (EPA, 1997a,b; releases, which were all together estimated to reach more than 11 Hammerschmidt et al., 2004; Balcom et al., 2004). This knowledge metric tons of mercury annually (NSTC, 2004). Other more diffuse has contributed to better regulation of mercury emissions. Despite sources include local and long-range atmospheric transport from these improvements, pollution of total mercury (tHg), mixture of global emissions (Wang et al., 2003). Studies show that wet and inorganic and organic mercury, from diffuse sources continue to dry atmospheric depositions are primary sources of mercury adversely affect aquatic food chains (EPA, 1997a). To date, public interest and research efforts on the distribution of Hg in the ⇑ Corresponding author. Tel.: +301 713 3028x132; fax: +301 713 4388. GOM have focused primarily on specific estuaries and embay- E-mail address: [email protected] (D.A. Apeti). ments, resulting in an extensive literature of localized extent
0025-326X/$ - see front matter Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.marpolbul.2012.08.006 2400 D.A. Apeti et al. / Marine Pollution Bulletin 64 (2012) 2399–2408
(Trefry et al., 2007; Tan, 2006). Integrated assessments of mercury box core. From each grab, the top three centimeter fraction of distributions throughout the GOM coastal waters are limited to a the sediment is sub-sampled with a Kynar coated scoop and placed few reports (Kim and Powell, 2001; Moore, 2000). It is important in a pre-labeled and pre-cleaned container. Sediments are collected to identify areas with potentially high methylation rates, as this from three separate stations to constitute a site composite sample. may have implications for human and ecosystem health. Such Detailed MWP sampling protocols are provided by Apeti et al. knowledge may allow coastal managers to develop targeted mon- (2011) and Lauenstein and Cantillo (1998). Because of deposition itoring plans for a better management of their coastal resources. rates, unlike bivalve tissues, sediment data are not conducive for Long-term monitoring data allow for the identification of areas of documenting short-term pollution trend. potentially high methylation across a wide geographic scale. The NOAA Mussel Watch Program (MWP) contaminant moni- 2.3. Oyster sampling toring data offers a unique opportunity for a comprehensive assessment of current status and temporal trends of mercury dis- Around the Gulf of Mexico, oysters are collected either by hand, tribution in the GOM. NOAA has collected mollusks and sediments using oyster-tongs, or via oyster-dredge, depending on the charac- in coastal waters nationwide since 1986, and has measured a broad teristics of the site and local oystering regulations. Oyster samples spectrum of chemical contaminants, including total mercury. In are sorted and 5 cm or more shell size organisms are selected. The 2006 and 2007, the Gulf of Mexico sediment and mollusk samples oysters are then cleaned with a nylon brush to remove detritus, were analyzed for both total mercury and MeHg. This paper offers and placed inside labeled double Ziploc bags. Samples are placed a broad geographic perspective of the mercury concentrations in on ice inside coolers until shipped to the analytical laboratory. the GOM and identifies areas of relatively elevated levels of MeHg Sampling frequency for bivalves has varied over the years. Samples and discusses long-term trends of total mercury in the GOM. were collected annually between 1986 and 1993, and biennially The US Environmental Protection Agency (EPA) has sponsored since 1994. From 1986 to 1991, three samples composites were two similar coastal monitoring programs. Each employed a strati- analyzed per site, but only one composite was analyzed thereafter. fied random sampling strategy rather than the Mussel Watch fixed A sample composite consisted of 20–30 individual oysters, station strategy used the NOAA program. From 1991 to 1994, EPA’s depending on oyster size. Environmental Management and Assessment Program (EMAP) sampled sediments and biota for contaminant analysis from the 2.4. Analytical methods Louisianan province of the Gulf of Mexico. From 2000 to 2004, EPA’s National Coastal Assessment program collected similar Individual oysters were cleaned, sized (length and weight), samples from throughout the coastal Gulf of Mexico. Neither EPA shucked, and composites of whole soft tissue homogenized. Sedi- program analyzed samples for MeHg. Rather than oysters, EPA ment samples were prepared by removing pebbles, shells, biota sampled biota such as fish and shrimp, whose mobility exposed and other detritus before being homogenized using a spatula. For them to mercury and other contaminants over potentially large tHg quantification, tissue and sediment samples were freeze dried areas, distant from the co-collected sediment samples. and approximately 0.3 g of homogenate was acid digested based on a modified version of the Environmental Protection Agency 2. Methods (EPA) method 245. Samples are digested using concentrated H2SO4 and HNO3 and the addition of KMnO4 and K2S2O8, followed by a 2.1. Sampling sites second heated digestion step. Before analysis, 5 mL of 10% (w/w) NH2OH. HCL were added to reduce excess permanganate and the The Mussel Watch Program monitors the status and trends of volume brought to 40 mL with distilled water. The detailed analyti- more than 150 chemical pollutants, including mercury, in US cal description is provided by Kimbrough and Lauenstein (2006). coastal waters. The program is based on the biennial collection For MeHg quantification, tissue and sediment samples were and analysis of sentinel bivalve mollusks (oysters and mussels), subjected to extraction and digestion techniques based on modi- with sediment samples collected approximately once every ten fied methods of Wagemann et al. (1997) and Uthe et al. (1972). years from approximately 300 nation-wide sites (Fig. 1). The Homogenates of the sample aliquots (0.2 g of tissue or 1.0 g of sed- program’s monitoring sites are labeled with four letter acronyms iment) were extracted into methylene chloride-hexane solvent that illustrate the site’s specific and general locations (Table 1). with potassium bromide and copper sulfate added to improve Along the GOM coastline, where the American oyster (Crassostrea extraction from the solid phases. The organic phase was digested virginica, Gmelin, 1791) is the primary sentinel organism, the in combusted glass vials, using nitric and sulfuric acids and potas- program has 87 long-term monitoring sites (Fig. 1). In 2006 and sium permanganate, in order to convert all mercury species to 2007, a total of 68 and 53 sites were collected for oysters and ionic mercury and to remove traces of organic solvent that would sediments, with the aim of assessing the current state of MeHg otherwise impact the measurement. This method measures total levels and its distribution in the GOM. The 68 Gulf MWP tissue MeHg, which is mostly composed of mono-methyl mercury with sites with monitoring data dating back to 1986 were used to assess trace amounts of dimethyl mercury. tHg long term temporal trends. Sample collection follows stringent In general, tHg and MeHg concentrations in sediment and tissue quality control protocols that are detailed in Apeti et al. (2011) and matrices were measured using cold vapor atomic fluorescence Lauenstein and Cantillo (1998). spectrometry at the Texas Element Research Laboratory. For tHg measurement, X-ray fluorescence and cold vapor inductively cou- 2.2. Sediment sampling pled mass spectrometry have been used in the past, particularly in 1990 and 1998, when three laboratories were conducting work Mussel Watch collects surficial sediment that is likely to repre- for the MWP (Lauenstein and Cantillo, 1998). However, variability sent newly deposited material. The average sedimentation rate in among analytical methods were minimized through the use of in- coastal environments was estimated to vary between 0.1and ter-laboratory exercises and performance based quality assurance 0.8 cm yÀ1 (Presley et al., 1998; Valette-Silver, 1992). Thus, to (QA) processes to ensure data quality. Typical method detection collect newly deposited sediments, MWP conducts sediment limits (MDL) for tHg in tissue and sediment samples were 0.004 sampling once every 10 years. At each station, fine-grained and 0.002 lggÀ1, respectively. The MDL for MeHg are 0.006 and sediments are collected using a van Veen sampler, or a hand held 0.003 lggÀ1 in tissue and sediment, respectively. Mussel Watch D.A. Apeti et al. / Marine Pollution Bulletin 64 (2012) 2399–2408 2401
Fig. 1. Map of the northern Gulf of Mexico depicting Gulf states, Mussel Watch monitoring sites, and some major rivers and bays. Inserted map depicts all Mussel Watch program monitoring sites in the continental US. data are reported on a dry weight (dw) basis, and are available on of Alabama, Mississippi and Louisiana; and the western Gulf, the web at http://www.ccma.nos.noaa.gov/stressors/pollution/ mainly Texas. nsandt/. Data quality was ensured by analysis of a series of quality The sediment and tissue data were mapped onto the three sub- control samples, including blanks and samples spiked with CH3- regions (eastern, central and western Gulf) based on statistical HgCl and certified reference materials such as the National Insti- assessment of the Gulf-wide tHg and MeHg data. Relationships be- tute of Standard and Technology’s (NIST) oyster tissue SRM-2976 tween tHg and MeHg concentration values in sediment and tissue and the European Community Bureau of Reference’s BCR sediment were assessed using Spearman rank correlation. Within each sub- CRM-580. region, Spearman correlation was further applied to the long-term For the Mussel Watch program, the analysis of the NIST oyster oyster tissue data for temporal evaluations of tHg concentrations tissue SRM-2976 and BCR sediment CRM-580 routinely yield for over two decades (1986–2009) of monitoring. Significance of recoveries of more than 90% for tHg. In this study, analyses of statistical tests were reported at the p = 0.05 level. SRM-2976 and CRM-580 yielded 84–95% and 92–113%, respec- tively, for MeHg. These analytical performances met data quality criteria of the National Status and Trends Program. 3. Results Although the oysters were not depurated prior to analysis, it is unlikely that gut contents contributed significantly to the measured 3.1. tHg and MeHg concentrations in oyster tissue mercury concentrations. Median tHg to iron ratios were 1.84 Â 10À6 6 and 326 Â 10À in sediments and tissues, respectively. Median Recent concentrations (2006/2007) of tHg and MeHg in oyster 6 6 MeHg to iron ratios were 0.169 Â 10À and 104 Â 10À in sediments tissues are presented in Tables 1a–c. Concentrations of tHg and and tissues, respectively. Undepurated sediments are likely to MeHg varied between 0.03 to 0.5 lggÀ1 dw and 0.01 to contribute <1% of the tHg and MeHg measured in oyster tissues. 0.2 lggÀ1 dw, respectively. Gulf-wide spatial distributions, based on cluster analysis, indicated that tissue tHg and MeHg concentra- 2.5. Statistical approach tions varied broadly along the northern GOM coastline (Figs. 2 and 3). Based on the cluster analyses, mercury ‘‘hotspots’’ were found Primary statistical analyses were conducted using JMP-5.1™ sys- in bays such as Florida, Tampa, Matagorda, and the Everglades. tem statistical package. The data were tested for normality using Intermediate concentrations were found in the coastal waters of Shapiro Wilks ‘‘goodness of fit’’ test. Because the data were not Florida and Texas, while the lowest tHg concentrations were pre- normally distributed, robust nonparametric statistical approaches valent along the coastlines of Louisiana, Mississippi and Alabama were utilized for data comparison and the assessment of temporal (Fig. 2). Aside from few sites in Tampa Bay, Florida and Matagorda and spatial changes. Multivariate cluster, hierarchical cluster analy- Bay, Texas with relatively elevated concentrations, MeHg spatial sis, with Ward’s minimum variance method, was conducted to distributions showed intermediate concentrations in Florida, while determine natural breaks within the concentration ranges. To assess low concentration values were found at the rest of the sites (Fig. 3). the spatial distributions, the concentration values for both tHg and In general, results for tHg in oyster tissue were within the range of MeHg were clustered into three categories to illustrate low, inter- published data. The Gulf of Mexico Program (GMP, 1999) mapped mediate and elevated or ‘‘hotspots’’ concentration ranges. Wilcoxon the Gulf-wide tHg concentrations in multiple marine species and rank-sum with Chi-square approximation tests were used to assess reported mean concentration of 0.6 lggÀ1 dw (0.08 lggÀ1 wet differences between cluster groups and sub-region comparisons. weight) in oysters. Also, tHg results in tissue were similar to data The northern GOM coastline displays geomorphologic differ- published by Kimbrough et al. (2008). ences (Schroeder and Wiseman, 1999) that can be grouped into The long-term (1986–2008) Mussel Watch monitoring data for three distinct and fairly uniform sub-regions: the eastern Gulf, tHg concentrations in oyster tissues (http://www.ccma.nos.noaa. predominantly Florida; the central Gulf, formed by the coastlines gov/stressors/pollution/nsandt) were utilized and sites with five 2402 D.A. Apeti et al. / Marine Pollution Bulletin 64 (2012) 2399–2408
Table 1a Concentration (lggÀ1 dry weight) of tHg and MeHg in oyster tissue and sediment samples collected during the 2006/2006 period at Mussel Watch sites in the Eastern GOM sub- region.
Site General location Specific location State Latitude Longitude Drainage area 2000 Census THg MeHg THg MeHg 20 km of the tissue tissue sediment sediment sites
AESP Apalachee Bay Spring Creek Florida 30.0633 À84.3220 Apalachee Bay EDA 15859 0.256 0.073 0.020 0.005 APCP Apalachicola Bay Cat Point Bar Florida 29.7242 À84.8842 Apalachicola Bay EDA 7104 0.144 0.028 0.022 MDL for MeHg in sediment was 0.003 lggÀ1. na Represents not analyzed (because sample were not collected). EDA stands for estuarine drainage area. Table 1b Concentration (lggÀ1 dry weight) of tHg and MeHg in oyster tissue and sediment samples collected during the 2006/2006 period at Mussel Watch sites in the Central GOM sub- region. Site General Specific location State Latitude Longitude Drainage area 2000 Census tHg MeHg THg MeHg location 20 km of the tissue tissue sediment sediment sites MBCP Mobile Bay Cedar Point Reef Alabama 30.3155 À88.1338 Mobile Bay EDA 15425 0.091 0.022 na na MBDR Mobile Bay Dog River Alabama 30.5917 À88.0398 Mobile Bay EDA 306497 0.080 0.030 na na ABOB Atchafalaya Bay Oyster Bayou Louisiana 29.2555 À91.1362 Atchafalaya/Vermilion Bays EDA 0 0.046 0.019 0.033 0.004 BBMB Barataria Bay Middle Bank Louisiana 29.2767 À89.9420 Barataria Bay EDA 1541 0.047 0.023 0.054 MDL for MeHg in sediment was 0.003 lggÀ1. na Represents not analyzed (because sample were not collected). EDA stands for estuarine drainage area. or more years of data were selected and used for the trend analysis. cally strong decreasing trend of tHg was observed in the eastern Temporal trends were assessed using non-parametric Spearman Gulf (Fig. 4b), with a decline of about 50% between 1986 and 2001. ranked correlation between year and tHg in oyster tissue at Gulf wide and sub-region scales (Fig. 4a and b). Spearman ranked corre- lations illustrated in Fig. 4a showed no specific decreasing or 3.2. Total mercury and methyl mercury concentrations in sediment increasing trends at the Gulf wide scale (q = À0.2, p > 0.05). How- ever, at the regional scale, the correlation assessment illustrated Recent concentrations (2006/2007) of tHg and MeHg in sedi- different relationships. Results for central and western sub-regions ments are presented in Tables 1a–c. Total mercury concentrations were similar to that of the Gulf wide assessment, while a statisti- in sediments varied between 0.01 and 0.2 lggÀ1 dw Gulf-wide. D.A. Apeti et al. / Marine Pollution Bulletin 64 (2012) 2399–2408 2403 Table 1c Concentration (lggÀ1 dry weight) of tHg and MeHg in oyster tissue and sediment samples collected during the 2006/2006 period at Mussel Watch sites in the western GOM sub- region. Site General location Specific location State Latitude Longitude Drainage area 2000 Census tHg MeHg THg MeHg 20 km of the tissue tissue sediment sediment sites ABLR Aransas Bay Long Reef Texas 28.0548 À96.9512 Aransas Bay EDA 20099 0.076 0.035 0.015 0.003 BRCL Brazos River Cedar Lakes Texas 28.8580 À95.4647 Brazos River EDA 37690 0.107 0.057 0.030 MDL for MeHg in sediment was 0.003 lggÀ1. na Represents not analyzed (because sample were not collected). EDA stands for estuarine drainage area. Similar ranges of tHg concentrations in sediment were found in northern GOM. Levels of tHg and MeHg in tissues and tHg in sed- EPA’s NCA Program (EPA, 2011). iment revealed a wide variability in the distribution of mercury Sediment MeHg concentrations were low, ranging mostly from across the monitoring area (Figs. 2, 3 and 5). For oyster tissue, undetected to a maximum concentration of 0.006 lggÀ1 dw, just elevated tHg and MeHg concentrations were found at sites or above the MDL (0.003 lggÀ1 dw). Because of these low values, ‘‘hotspots’’ mostly located in the eastern Gulf (Fig. 2). However, MeHg concentrations in sediment are not extensively discussed some hotspots with elevated tissue tHg and MeHg concentrations in this paper. Nonetheless, it is noteworthy that MeHg concentra- were also found along the coastlines of the western and central tions above the MDL were more prevalent in sediment samples Gulf (Tables 1a–c). Current mercury concentrations in the GOM collected along the coastal waters of Louisiana (Table 1b). were slightly higher than the national medians derived from the The spatial distribution of tHg in sediments is illustrated in National Status and Trend monitoring data for both oysters and Fig. 5. Pockets of relatively elevated tHg concentrations were sediment. While elevated mercury concentrations are present else- observed across the study area. Total mercury concentrations in where in the Nation’s coastal waters (Kimbrough et al., 2008), the sediment were elevated at sites in Matagorda and Galveston Bays, Gulf of Mexico is home to some of the most elevated mercury Texas. The highest concentrations Gulf-wide were found in Tampa concentrations. Bay, Florida. Intermediate to low tHg concentration values were Many of the highest tHg and MeHg concentrations in both oys- distributed all along the other areas of the Gulf coast. In contrast ters and sediments are found in remote rural areas. To assess to the Gulf-wide distributions of tHg in oyster tissues, tHg impacts of population density on the distribution of mercury sediment concentrations appeared to be more uniformly distrib- concentrations along the Gulf coastal environment, the 2006/ uted in sediments across the entire Gulf, with no significant 2007 tissue concentrations were correlated to the 2000 census sub-regional concentration differences (p > 0.05). We explored data within 20 km of the MW sites (Fig. 6). The Spearman statistic normalization of tHg to measures of sediment texture, aluminum revealed no significant correlations suggesting that the distribu- concentrations and total organic carbon concentrations to reduce tions of tHg and MeHg in the Gulf coastal waters may be largely variability and enhance any signal influencing bioavailability. independent of human population density (Fig. 6). Scudder et al. Such relationships were absent, similar to earlier studies (Daskal- (2009), looking at freshwater streams across the country, found akis and O’Connor, 1995; Hanson et al., 1993; Windom et al., that mercury accumulation in fish was negatively related to the 1989). A similar absence of such relationships was observed for urban character of the stream, suggesting the generality of the lack MeHg. of an urban influence. There is evidence of the influence of point source mercury contamination in several estuaries. Elevated concentrations of 4. Discussion tHg and MeHg are found in oysters and sediments of Matagorda Bay (Figs. 2, 3 and 5), which can be linked to historical industrial 4.1. Spatial distribution activity. The mercury hotspot in Matagorda Bay is located in Lavaca Bay, a sub-estuary identified as an EPA superfund site, which was The MWP sediment and tissue data give a broad perspective of heavily polluted with mercury contaminated effluents from a the geographical distribution of mercury in coastal areas of the chlor-alkali facility at Point Comfort, Texas, in the late 1960s 2404 D.A. Apeti et al. / Marine Pollution Bulletin 64 (2012) 2399–2408 (EPA, 2001). The legacy of that historic contamination remains. The importance of mercury species concentrations and extract- Contamination from a similar facility contributed to elevated ability are likely to be linked to geographical differences among mercury concentrations in Lake Calcasieu, Louisiana. Gulf sub-regions through watershed and estuarine processes, and Mercury contamination is not uniformly distributed within attributes that characterize these sub-regions. In this regard, the estuaries with multiple MWP sites (Table 1a–c). Tampa Bay best eastern and central sub-regions differ most. The central sub-region exemplifies this, with highest tHg and MeHg concentrations in is dominated by the influence of the Mississippi River and its drain- oysters at sites inside sub-embayments, where restricted water age, with high suspended sediment loads and introduction of circulation and potentially enhanced mercury methylation would nutrients stimulating high phytoplankton productivity. Water- favor increased MeHg and its bioavailability. sheds extend inland to higher elevations, which facilitates soil The bioaccumulation of MeHg and inorganic mercury by oysters and sediment erosion and suspended particle delivery to estuaries. is expected to occur largely in the process of filtering food particles This is evident in satellite images showing sediment plumes from water. The assimilation of mercury by oysters depends on the extending into the Gulf of Mexico from not only the Mississippi concentration of the mercury species associated with phytoplank- River but also the Atchafalaya River and Mobile Bay. The conse- ton and non-living particles and the ease with which the mercury quence of high sedimentation rate (0.8 cm/year) (Presley et al., species can be extracted from the solid substrates (Gagnon and 1998) in the Mississippi River Delta is that sediments delivered Fisher, 1997). Bioaccumulation is also possible directly from solu- to central Gulf estuaries will dilute mercury from recent atmo- tion, but is thought to be of lesser importance. spheric deposition with material of lower mercury concentrations. Fig. 2. Distribution of tHg concentrations in northern GOM coastal waters based on measurements in oyster tissue collected in 2006/2007. Grouping in the concentration values were based on cluster analysis. Fig. 3. Distribution of MeHg concentrations in northern GOM coastal waters based on measurements in oyster tissue collected in 2006/2007. Grouping in the concentration values were based on cluster analysis. D.A. Apeti et al. / Marine Pollution Bulletin 64 (2012) 2399–2408 2405 Moreover, the older, eroded material is likely to contain mercury of environmental concentrations. Water retention times in eastern reduced reactivity and bioavailability (Orihel et al., 2008). The Florida Bay, for example, may be as long as half a year (Lee et al., higher phytoplankton productivity, also visible in satellite imagery 2006). of the central region coast and estuaries, will encourage secondary The differences in MeHg concentrations between the central production of oysters and other biota, but at the cost of diminution and eastern sub-regions can be seen in comparing values from of mercury concentrations through growth dilution (Chen and Folt, peninsular Florida and the Mobile Bay drainage. Bergamaschi 2005). et al. (2012) reported filter MeHg concentrations in water from By contrast, estuaries from the eastern sub-region, especially southwest Florida rivers, with a median value of 2.39 ng LÀ1 along the Florida peninsula, drain small, low lying coastal plain and an extraordinary maximum value of 26.8 ng LÀ1. By contrast, watersheds. River flows are generally modest, and deliver recent results for filters in the central region, such as Mobile Bay’s atmospheric mercury deposition without the lengthy sediment drainage, had a median concentration of 0.09 ng LÀ1, and a max- particle contact times that reduce mercury bioavailability. In addi- imum concentration of 1.47 ng LÀ1 (Warner et al., 2005). The tion, these coastal watersheds contain a high percentage of wet- importance of watershed type and extent can be seen in South lands, 95% of the watershed of Florida Bay, 84% and 67% in South Carolina, where MeHg in both water and resident biota are high- and North Ten Thousand Islands, respectively. Other watersheds er in coastal plain watersheds, of largely local source water, than in the eastern sub-region average about 10% wetlands (Bricker in Piedmont and upland watersheds (Glover et al., 2010; Bradley et al., 2007). By contrast, the Mississippi River watershed is about et al., 2010) 1% wetlands, Mobile Bay 2% and Atchafalaya 6%. Wetlands are a widely recognized source of MeHg to the waters into which they 4.2. Relationships between tHg and MeHg drain. This may contribute to the higher MeHg concentrations ob- served in oysters from the eastern sub-region. The generally lower Methyl mercury content in oyster tissues varied greatly Gulf- freshwater delivery rates from the small watersheds of this region, wide (Tables 1a–c). Concentrations of tHg and MeHg in tissues combined with shallow estuarine depths, mean that MeHg pro- were strongly correlated (Fig. 6). The MeHg/tHg ratio (%MeHg) in duced within such estuaries is diluted less and retained for longer sediments has been suggested to serve as a surrogate for mercury periods allowing for resident oysters to be exposed to higher MeHg methylation potential in sediments (Drott et al., 2008). We lacked (a)0.25 (b) ρ = -0.2 0.25 p = 0.10 0.20 0.20 0.15 0.15 0.10 0.05 0.10 tHg in tissue (ug/g dw) ρ = -0.73 tHg in tissue (ug/g dw) dw) (ug/g tHg in tissue p = 0.0001 0.00 0.05 1985 1990 1995 2000 2005 2010 1985 1990 1995 2000 2005 2010 Year Year Fig. 4. tHg trend assessment in the GOM based on long-term (1986–2009) oyster tissue concentrations; (a) Gulf-wide assessment showing no trend, which is similar to the central and western sub-regions and (b) depicts a statistically significant decreasing trend in the eastern Gulf sub-region. Fig. 5. Distribution of tHg concentrations in northern GOM coastal waters based on measurements in sediments collected in 2006/2007. Groupings in the concentration values were based on cluster analysis. 2406 D.A. Apeti et al. / Marine Pollution Bulletin 64 (2012) 2399–2408 (a) 0.5 (b) 0.5 (c) 0.25 ρ = 0.82 ρ = 0.25 ρ = 0.23 p < 0.001 p = 0.04 p = 0.05 0.4 0.4 0.20 0.3 0.3 0.15 0.2 0.2 0.10 0.1 0.1 0.05 tHg intHg tisue (ug/g dw) tHg intHg tisue (ug/g dw) MeHg in tisueMeHg (ug/g dw) 0.0 0.0 0.00 0.00 0.05 0.10 0.15 0.20 0.25 200x103 400x103 600x103 800x103 1x106 200x103 400x103 600x103 800x103 1x106 MeHg in tissue (ug/g dw) 2000 human population at 20 km around sites 2000 human population at 20 km around sites Fig. 6. Scatter plots depicting relationships between (a) tHg/MeHg; (b) tHg/2000 census and (c) MeHg/2000 census. The 2000 census used is human population within 20 km radius of Mussel Watch sites. The strength of the relationships was assessed with non-parametric Spearman correlation. sufficient sensitivity in our MeHg measurements in sediments to Because sediment and oyster sites are co-located or placed in apply this concept to define potential mercury methylation hot- close proximity of each other in the same water body, one would spots in Gulf estuaries. However, by extension, it seems possible expect strong relationships between mercury concentration in oys- to employ %MeHg in oysters to attempt a similar assessment. ter tissue and sediment. The statistical determination for the rela- MeHg/tHg ratios were calculated for each bay sampled in 2006 tionship between sediments and oyster tissues for MeHg was not and 2007 (Table 2). The maximum %MeHg (56.4%) value in oysters feasible because of frequent sub-MDL MeHg concentrations in was found in Rookery Bay in Florida. However, ratios exceeding sediments (Tables 1a–c). However, the poor correlation between 40% were found in all sub-regions. Rather than reflecting mercury tHg concentrations in tissue and sediment (Fig. 6), may be due to methylation potential, in the central region especially, high ratios the fact that oysters are filter feeders and are mainly exposed to seem to result from the low concentrations of tHg in oysters, which contaminants that are in suspension in the water column. Gener- would be the result of generally lower bioavailability of both tHg ally, contaminant bioaccumulation in oysters depends on com- and MeHg in this sub-region. MeHg is certainly known to be pro- bined abiotic and biotic factors that involve contaminant duced readily in sediments of the central Gulf region (Hall et al., concentration, chemical speciation, diffusion and sediment resus- 2008). pension (Roesijadi, 1996). Thus for tHg, the poor relationship Table 2 Bay-specific MeHg/tHg percentages ratio in tissue are derived based on median tHg and MeHg concentrations values calculated for each water bodies. Bay Sub-region Residence time* (d) Median tHg tissue Median MeHg tissue Median tHg sediment MeHg/tHg % ratio tissue Rookery Bay Eastern NA 0.25 0.14 0.01 56.4 Espiritu Santo Western NA 0.07 0.04 0.02 55.7 Naples Bay Eastern NA 0.13 0.07 0.02 52.7 Lower Laguna Madre Western NA 0.08 0.04 0.01 52.3 Brazos River Western NA 0.09 0.05 0.02 51.0 San Antonio Bay Western 40 0.07 0.03 0.01 50.7 Everglades Eastern NA 0.19 0.10 0.02 50.3 Barataria Bay Central 120 0.04 0.02 0.05 46.4 Aransas Bay Western 350 0.08 0.03 0.01 46.0 Caillou Lake Central NA 0.03 0.01 0.05 42.6 Atchafalaya Bay Central 5 0.05 0.02 0.03 42.0 Galveston Bay Western 40 0.05 0.02 0.04 41.1 Mississippi Sound Central 75 0.09 0.04 – 39.6 Choctawhatchee Bay Eastern 40 0.12 0.05 0.06 39.4 Florida Bay Eastern NA 0.22 0.09 0.02 39.1 Terrebonne Bay Central 115 0.05 0.02 – 35.7 Corpus Christi Western 350 0.12 0.04 0.04 34.8 Matagorda Bay Western 75 0.10 0.03 0.02 33.8 Tampa Bay Eastern 150 0.15 0.05 0.02 33.8 Calcasieu Lake Central 30 0.11 0.04 0.04 33.5 Lake Borgne Central 20 0.05 0.02 – 31.9 Mesquite Bay Western NA 0.07 0.02 0.02 30.8 Joseph Harbor Bayou Central NA 0.06 0.02 0.06 30.8 Mobile Bay Central 10 0.09 0.03 – 30.6 Charlotte Harbor Eastern 63 0.18 0.05 0.01 30.4 Breton Sound Central 115 0.07 0.02 – 30.2 Sabine Lake Central 10 0.12 0.03 0.02 29.1 Apalachee Bay Eastern 25 0.26 0.07 0.02 28.6 Suwannee River Eastern 3 0.11 0.03 0.07 26.4 Pensacola Bay Eastern 26 0.13 0.03 0.05 26.2 Copano Bay Western NA 0.10 0.03 0.02 25.6 Vermilion Bay Central 5 0.05 0.01 0.04 24.5 Apalachicola Bay Eastern 10 0.13 0.03 0.04 21.1 Cedar Key Eastern NA 0.17 0.03 0.02 18.9 St. Andrew Bay Eastern 26 0.14 0.02 – 17.1 NA indicates not available. * Data derived from Solis and Powell (1999). D.A. Apeti et al. / Marine Pollution Bulletin 64 (2012) 2399–2408 2407 between tissue and sediment concentrations may be the result of and its delivery to estuaries, it will be difficult to observe improve- such complex factors as the mercury oxidation state, methylation ments in the desired outcome of reduced mercury bioaccumula- and uptake rate of oysters (Kannan et al., 1998; Benoit et al., 2006). tion in coastal areas of the Gulf of Mexico in the short-term. 4.3. Toxicity implications 5. Conclusion Mercury species, such as monomethyl mercury, have no known The intent of the MWP is to monitor trends and discover biological function, and are potentially hazardous to exposed changes in contamination based on analysis of sediments and bi- organisms. Accumulation of mercury above background levels in valves over time. The concurrent analyses of tHg and MeHg in this aquatic systems can pose serious environmental threats to wildlife assessment provide relevant information on the current status of (EPA, 1997a,b; Muir et al., 2005). Toxic effects of mercury, particu- the distribution of tHg and MeHg concentrations in the coastal larly those of MeHg, are well documented (Mastromatteo and areas of the northern GOM. Spatial distribution assessment of Sutherland, 1972; ATSDR, 1999). Signs of neurological diseases, tHg and MeHg in both sediment and oyster tissues indicated a including abnormal behavior, convulsion, reduced fitness and broad range of mercury concentrations across the northern GOM, death, have been observed in wildlife of higher taxa than oysters with sub-regional differences which may be linked to a host of di- exposed to MeHg (EPA, 1997a,b; Murphy et al., 2008). In humans, verse factors, ranging from local point sources to atmospheric MeHg is a potent neurotoxin that can affect developing fetuses and transport, coastal environment type and weather patterns. In gen- their brain development, as well as cause kidney damage and eral, tHg concentrations in oyster tissues were low relative to the autoimmune disorders (EPA, 1997a,b; Moore, 2000). To minimize FDA action level in seafood. Based on the long-term NS&T Mussel human exposure through seafood consumption, the US Food and Watch data, tHg in tissues show fairly static temporal trends along Drug Administration (FDA) has set the maximum permissible level the central and western Gulf coast, while a strong decreasing trend À1 of 1 lgg MeHg wet weight (ww) in fish and shellfish. EPA em- was observed in the eastern Gulf. However, mercury hotspots in À1 ploys a criterion of 0.3 lgg ww at a standard meal size and fre- estuaries that support important recreational and commercial fish- quency. Using 85% as the moisture content for oysters (average eries indicate that mercury is still a concern in the GOM. A sus- value derived from Mussel Watch measurements), the Mussel tained monitoring and research effort is needed to continue to Watch monitoring tHg data in oyster tissues from the Gulf of Mex- provide relevant information for a better management of the mer- ico were well below guidelines. However, because mercury can cury issue in the GOM. biomagnify up food webs (Mastromatteo and Sutherland, 1972), low concentrations observed in bivalves, which are near the Acknowledgment bottom of estuarine food webs, could translate into higher concen- trations in apex predators such as fish, birds and humans. Oysters The authors are grateful to Dr. Robert Taylor of the Texas Ele- are of value as sentinels and can be predictors of such potential ment Research Laboratory for performing the analytical chemistry consequences. In fact, the sub-regional pattern of high mercury for this study. Also, we would like to acknowledge Kevin McMahon concentrations in oysters from the eastern Gulf of Mexico, and and Terry McTigue for their critical review and helpful comments. lowest concentrations in the central sub-region, is mirrored in the pattern of mercury concentrations in a broad range of estuarine fish species reported in Ache et al. (2000): spotted seatrout, red Appendix A. Supplementary data drum, hardhead and gafftopsail catfish, Gulf flounder, and sheeps- head. This concurrence argues that the sub-regional patterns are Supplementary data associated with this article can be found, in not species specific, but a reflection of common underlying the online version, at http://dx.doi.org/10.1016/j.marpolbul. environmental levels. 2012.08.006. 4.4. Temporal trends References There is an indication of a slow decreasing trend for tHg concen- Ache, B.W., Boyle, J.D., Morse, C.E., 2000. 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