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. Author manuscript; available in PMC: 2020 Oct 15.
Published in final edited form as: Sci Total Environ. 2019 Jun 7;687:907–916. doi: 10.1016/j.scitotenv.2019.06.094

Effects of Temperature, Salinity, and Sediment Organic Carbon on Methylmercury Bioaccumulation in an Estuarine Amphipod

Amanda N Curtis a,1,*, Kimberly Bourne b, Mark E Borsuk b, Kate L Buckman a, Eugene Demidenko c,d, Vivien F Taylor e, Celia Y Chen a
PMCID: PMC6697058  NIHMSID: NIHMS1532527  PMID: 31412494

Abstract

Mercury (Hg) is a global contaminant that poses a human health risk in its organic form, methylmercury (MeHg), through consumption of fish and fishery products. Bioaccumulation of Hg in the aquatic environment is controlled by a number of factors expected to be altered by climate change. We examined the individual and combined effects of temperature, sediment organic carbon, and salinity on the bioaccumulation of MeHg in an estuarine amphipod, Leptocheirus plumulosus, when exposed to sediment from two locations in the Gulf of Maine (Kittery and Bass Harbor) that contained different levels of MeHg and organic carbon. Higher temperatures and lower organic carbon levels individually increased uptake of MeHg by L. plumulosus as measured by the biota-sediment accumulation factor (BSAF), while the effect of salinity on BSAF differed by sediment source. Multi-factor statistical modeling using all data revealed a significant interaction between temperature and organic carbon for both sediments, in which increased temperature had a negative effect on BSAF at the lowest carbon levels and a positive effect at higher levels. Our results suggest that increased temperature and carbon loading, of a magnitude expected as a result from climate change, could be associated with a net decrease in amphipod BSAF of 50 to 71%, depending on sediment characteristics. While these are only first-order projections, our results indicate that the future fate of MeHg in marine food webs is likely to depend on a number of factors beyond Hg loading.

Keywords: Ocean warming, Leptocheirus plumulosus, Multi-factor models, Estuary, Bioaccumulation

1. INTRODUCTION

Mercury (Hg) is a global contaminant with an increased presence in the biosphere due to human activity, particularly from the burning of coal (Hsu-Kim et al., 2018; Obrist et al., 2018; Streets et al., 2017; UNEP, 2013). Mercury is listed third on the Comprehensive Environmental Response, Compensation, and Liability Act (CERCLA) Priority List of Hazardous Substances (ATSDR, 2017) and in its organic form, methylmercury (MeHg), poses potential toxicity with neurological, immunological, and cardiovascular effects (Eagles-Smith et al., 2018; Karagas et al., 2012; Mahaffey et al., 2011; Mergler et al., 2007; Nyland et al., 2011). Consumption of fish and shellfish is the dominant route of exposure to MeHg (Sunderland, 2007; Sunderland et al., 2018); therefore, MeHg-contaminated fish pose a serious public health concern. Currently, all U.S. states have Hg fish consumption advisories, including coastal advisories for the Atlantic coast and the Gulf of Mexico (Taylor and Williamson, 2017).

As many commercially important fish and shellfish species use estuaries as nursery grounds (Beck et al., 2001) and because approximately 87% of the global wild fish/shellfish harvested for human consumption comes from marine systems (FAO, 2016), it is particularly important to understand the controls on Hg in estuarine ecosystems. The cycling and fate of Hg in estuaries is known to be controlled by biological, physical, and chemical processes that are strongly influenced by water temperature, carbon availability, and salinity (Dijkstra et al., 2013; Driscoll et al., 2012; Schartup et al. 2013; Maulvault et al., 2016; Jonsson et al. 2017; Maulvault et al., 2017; Schartup et al. 2018) - all of which are expected to be impacted by climate change (Allison and Bassett, 2015; Doney, 2013; Karl et al., 2009; Rabalais et al., 2009; Scavia et al., 2002). Within estuarine systems, microbes transform Hg into MeHg and then MeHg is bioaccumulated at the base of the food chain (e.g., phytoplankton or benthic algae) and biomagnifies up the food web (e.g., Heyes et al. 2006; Chen et al. 2014). To examine how environmental factors could alter the transfer of mercury (Hg) from sediments to organisms at the base of the food chain, we worked with the amphipod, Leptocheirus plumulosus, a benthic invertebrate commonly used for sediment toxicity tests (US EPA, 1994). L. plumulosus burrows in sediments and feeds on organic matter in the sediment, but predominantly feeds on water column particulates that settle on the sediment surface (Taylor et al. 2014). Additionally, L. plumulosus is an important prey item for other invertebrates and forage fish comprising between 14–71% of the summer diet of common estuarine species found along the Eastern U.S. (e.g., Blue crab (Callinectes sapidus), Spot (Leiostomus xanthurus), Atlantic croaker (Micropogonias undulates), and Hogchoker (Trinectes maculatus)) (Hines et al., 1990) and thus represents an important link in the trophic transfer of Hg (~74% of MeHg from L. plumulosus was retained in predatory mummichogs (Goto and Wallace, 2009)).

The goal of this study was to experimentally investigate how changes in temperature, carbon, and salinity individually and in concert, influenced MeHg uptake in the benthic invertebrate, L. plumulosus. While prior studies have inferred the individual influence of these factors on MeHg production, flux, and uptake (Alava et al. 2017; Alava et al. 2018; Benoit et al., 2003; Hammerschmidt and Fitzgerald, 2004; Hammerschmidt et al., 2008; Heyes et al., 2006; Hollweg et al., 2009; Hollweg et al., 2010; Kim et al., 2008; Lawrence and Mason, 2001; Taylor et al., 2014; Williams et al., 2010), there are few experimental studies that investigate their combined effect on overall bioaccumulation. Further, the studies that have examined multiple stressors on MeHg bioaccumulation have found complex interactions (Buckman et al., 2019). We exposed the benthic estuarine amphipod, Leptocheirus plumulosus, to sediments collected from two sites in the Gulf of Maine to address the following research questions: 1) How do temperature, sediment organic carbon content, and salinity individually affect bioaccumulation of MeHg? 2) Do temperature, sediment organic carbon, and salinity have interacting effects on bioaccumulation? 3) Do these individual and interacting effects differ between sediment types?

2. MATERIALS AND METHODS

2.1. Sediments

Prior to the start of each experiment, sediment collected from Wells, ME that was low in MeHg (0.27–0.67 ng/g; Table S1) was used to acclimate L. plumulosus to environmental conditions. For the experimental manipulations, we used two sediments, different in Hg concentration and organic makeup, from Kittery, ME and Bass Harbor, ME, both located in the Gulf of Maine (Table 1). Kittery, ME is the site of the Portsmouth Naval Shipyard at the mouth of the Piscataqua River connecting Great Bay Estuary to the Gulf of Maine. It is an industrialized site known to have elevated levels of contaminants, including Hg in estuarine sediments and biota (Jones, 2000). Bass Harbor is an estuary located in Acadia National Park for which the primary source of Hg is atmospheric deposition (Bank et al., 2007). Despite its distance from direct Hg sources, it has relatively high concentrations of dissolved MeHg (Taylor et al., 2019).

Table 1.

Sediment characteristics for Kittery and Bass Harbor, range of sediment MeHg (ng/g) and range of sediment %LOI.

Site Site characteristics Sediment MeHg (ng/g) Sediment %LOI
Kittery Fine grained anoxic sediments with little surrounding marsh; surrounded by industrial development and adjacent to Portsmouth Naval Shipyard 0.36–1.85 5.26–8.90
Bass Harbor Fine grained anoxic sediment surrounded by extensive salt marsh; located adjacent to Acadia National Park 0.31–0.88 8.07–12.30
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2.2. Single-factor experiments

In single-factor experiments, only one environmental factor was manipulated at a time over the following range of values: temperature (12–30°C), sediment organic carbon (1.6–8.0 percent loss on ignition, % LOI), and salinity (0–40 ppt) (Figure 1). We examined a wide range of temperatures, carbon, and salinity in order to fit statistical models that could be used to assess how changes in these variables could result in changes in MeHg bioaccumulation.

Figure 1.

Figure 1.

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Experimental conditions for single-factor experiments for temperature, sediment organic carbon, and salinity for Kittery and Bass Harbor sediments. Each container held ~2 cm of sediment to which 800–1000mL of salt water and 30–50 amphipods were added. Each experimental condition was replicated using three containers, however due to occasionally low amphipod survival for Kittery, multiple blocks were used. Samples denoted with a * are those that were pooled or not included in statistical analyses (see Table S3 for %survival). acarbon at 6.5%LOI and 20ppt salinity, bcarbon at 10%LOI and 20ppt salinity, ctemperature at 22C and 20ppt salinity, dcarbon at 6.5%LOI and 22° C, ecarbon at 8.0%LOI and 22° C

Prior to the start of each experiment, approximately two centimeters of sediment was added to plastic containers (1.5L) filled with Instant Ocean (Spectrum Brands, Inc., Blacksburg, VA) saltwater (800–1000mL), with Tetramin® (Spectrum Brands, Inc., Blacksburg, VA) sprinkled to stimulate microbial activity. For temperature and salinity experiments, unamended sediment (<425μm sieved) was used, but for the carbon experiments, sand (sieved at <425μm) was mixed with sediment to create varying levels of organic carbon. The amount of organic carbon, hereafter, %LOI was determined by calculating the difference in weight before and after heating at 550°C for 6 hours in a muffle furnace (Schulte and Hopkins, 1996). For temperature and carbon experiments, salinity was held at 20 ppt. For salinity and carbon experiments, temperature was held at 22°C. For temperature and salinity experiments, organic carbon was held at approximately 6.5% LOI for Kittery and 8–10% LOI for Bass Harbor. Lids were placed on the top of the containers to minimize evaporation, containers were aerated, and sediments were allowed to equilibrate and settle for one week in environmental growth chambers (16h light: 8h dark) at 22°C for salinity and organic carbon experiments, or at the designated temperature for the temperature experiments, prior to addition of amphipods.

Stock cultures of L. plumulosus maintained at Dartmouth College were sieved at 850μm to select only juvenile and adult amphipods in order to obtain sufficient biomass for MeHg analysis and to utilize amphipods of a size that would be commonly consumed by predators in order to assess their role as prey items in transferring MeHg. For carbon experiments, 30 to 50 L. plumulosus individuals (for adequate biomass) were added to experimental sediment containers immediately after harvest from the stock cultures. For salinity and temperature experiments, L. plumulosus were acclimated to experimental conditions for 3–5 days prior to addition to experimental containers. To assess the pre-exposure level of MeHg in L. plumulosus, three samples of acclimated culture animals were collected at the start of the experimental set-up and analyzed for MeHg (Table S1).

Exposures lasted four weeks with complete water changes three times per week. For salinity experiments, salinity was checked daily to verify <1 ppt variation, and for temperature experiments, containers were rotated among chambers to eliminate chamber effects. L. plumulosus were not fed any additional food during the course of the experiment so that all available food was contained in the sediment. At the conclusion of the experiment, buckets were sieved at 850 μm to harvest amphipods, which were depurated overnight and counted to calculate percent survival. The collected amphipods were placed in trace metal clean vials to obtain wet weight, samples were frozen at −20°C, freeze dried, reweighed to obtain dry weight, and then homogenized prior to MeHg analysis. In cases of low survival, replicates were pooled to have sufficient material for MeHg speciation analysis. Sediments were settled overnight, overlying water was poured off and then sediments were homogenized, sub-sampled, frozen at −20°C, and then freeze-dried at prior to MeHg analysis.

All treatments were replicated using triplicate containers, however due to low survival, we pooled amphipods at the conclusion of the experiment to have sufficient biomass for MeHg analysis (Table S3, Figure 1). For some experiments, especially those with low survival or to examine a finer scale difference between treatments (i.e. 25°C vs. 27°C vs. 30°C), multiple treatment blocks were used. More specifically, for single-factor experiments that assessed temperature and carbon using Kittery sediment two blocks of experiments were used, with each temperature or %LOI replicated three times. For the salinity experiment using Kittery sediment, three blocks of experiments were used, but due to very low survival in one experiment at salinity <9ppt, these values were eliminated from statistical analysis. Single-factor experiments using the Bass Harbor sediments used single trials, as we had a priori information about the relevant ranges of variables (carbon, salinity and temperature) and because amphipod survival was high.

2.3. Two-factor experiments

Two-factor experiments to assess interactions between variables were performed using the same experimental procedures described above, but with two factors (carbon × temperature or carbon × salinity) simultaneously manipulated. For the carbon × temperature experiments, sediments were mixed to create a range of 1–6% LOI for Kittery and 1–10.9% LOI for Bass Harbor and then haphazardly placed at 15°C, 20°C, or 25°C (Figure 2). We ran three trials of carbon × temperature experiments and two trials of carbon × salinity experiments, in which each carbon-temperature or carbon-salinity interaction was replicated in triplicate and, if survival was low in these replicates, samples were pooled (see Table S3, Figure 2) to provide sufficient biomass for MeHg analysis. We collected sediment samples for Hg analysis both prior to the initial set-up and at the conclusion of the experiment to examine whether sediment Hg concentrations changed over the course of the experiment. While there were some differences, they were consistent with uptake from L. plumulosus (Table S2). For a separate more limited number of carbon × salinity experiments, Bass Harbor sediment was mixed with sand to be comparable in %LOI to the Kittery sediment (approximately 6.5% LOI) and then exposed to a range of 5–30 ppt salinity.

Figure 2.

Figure 2.

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Experimental conditions for two-factor experiments for temperature × carbon and salinity × carbon for Kittery and Bass Harbor sediments. Each container held ~2 cm of sediment to which 800–1000mL of salt water and 30–50 amphipods were added. Each experimental condition shown was replicated using three containers, however due to occasionally low amphipod survival, multiple blocks were used. Samples that are denoted with a * indicate those that were pooled or not included in statistical analyses (see Table S3 for %survival). asalinity held at 20ppt, btemperature held at 22° C

2.4. MeHg Analysis

The mean dry weight of all amphipod samples was 0.0335 g, with a range of 0.0016–0.2208 g, where the smaller weights were from the treatments with lower survival. Freeze-dried amphipods and sediments were spiked with enriched Me201Hg (Taylor et al., 2008); amphipods were extracted with 25% tetramethylammonium hydroxide (TMAOH), and sediments were leached with potassium bromide (KBr)/sulfuric acid (H2SO4)/copper sulfate (CuSO4) and back-extracted with dichloromethane (Bloom et al., 1997). Samples were analyzed by automated purge and trap gas chromatograph (GC) (MERX-M, Brooks Rand Instruments, Seattle, WA) coupled with inductively coupled plasma mass spectrometry (ICP-MS) (Agilent 7700x; Agilent Technologies, Santa Clara, CA) at the Dartmouth Trace Element Analysis Core using a method similar to EPA method 1630 (Taylor et al., 2011). Method detection limits were 1.0 ng/g for amphipod MeHg and 0.1 ng/g for sediment MeHg. Percent recovery of MeHg from SRM (DORM-4 or mussel) averaged 97.94 ± 8.50% (range: 78.4–110%) relative to certified value (355 ng/g), and relative percent difference from sample duplicates averaged 1.25 ± 1.09% (range: 0–3%) for amphipods. For sediments, MeHg recoveries relative to in-house standards averaged 106.8 ± 7.50% (range: 96–121%) and sediment duplicates averaged 9.06 ± 11.21% difference (range: 0–42.5%).

2.5. Statistical Analysis

To compare across experiments, we calculated the biota-sediment accumulation factor (BSAF) by dividing amphipod MeHg concentration by sediment MeHg concentration. Samples that had <50% survival were removed from analysis to avoid including data from organisms that may have been stressed (Table S3). For treatments where replicates of amphipods were pooled, the mean MeHg values of the corresponding sediments were used to calculate the BSAF.

The relationships between environmental conditions and amphipod MeHg, sediment MeHg, and BSAF were assessed using linear regressions with mixed effects using the lmer function in the statistical package R (Bates et al., 2015). Container effects were considered as a random effect for all models. Prior to analysis, the response variables were natural log-transformed to better meet the assumptions of regression. Single-factor analysis was performed for all three response variables (BSAF, sediment MeHg concentration, and amphipod MeHg concentration), while only BSAF was modeled in the multi-factor analysis.

Multi-factor analysis allows all the data for each location’s sediment to be analyzed simultaneously, thus enhancing statistical power and allowing for interactions. Random effects attributed to container effects were included in the model. Linear terms for salinity, temperature, organic carbon (%LOI), and all possible interaction terms were included as possible predictors. All combinations of these predictor variables were assessed for model performance. A model was fit using all hypothesized predictor variables, then any predictor variables that were not significant in either model were removed. This resulted in a final model that included %LOI, temperature, and the interaction of %LOI × temperature. Additionally, each factor was assessed for statistical significance using a t-test with a threshold p-value of 0.1. A relatively large p-value was used because our purpose was to develop an explanatory and predictive model and not to test hypotheses per se.

3. RESULTS AND DISCUSSION

3.1. Single factor experiments

In the single-factor experiments, amphipods exposed to both the Hg contaminated (Kittery) and relatively pristine (Bass Harbor) sediments responded to temperature in a similar manner: higher temperature resulted in greater bioaccumulation (Kittery: r2=0.72, p = 0.0003; Bass Harbor: r2=0.50, p= 0.084; Table 2, Figure 3), with no corresponding changes in sediment MeHg concentration (Kittery: r2=0.008, p =0.65; Bass Harbor: r2=0.04, p=0.50; Table 2, Figure 3). This produced much greater BSAF values at high temperatures for amphipods in the Kittery sediment, but not a significant effect in the Bass Harbor sediment (Kittery: r2=0.42, p =0.0084; Bass Harbor: r2=0.26, p=0.18; Table 2, Figure 3). Previous research has shown that, over a range of natural temperatures in salt pools, bioaccumulation of MeHg was higher in killifish (Fundulus heteroclitus) in pools with higher temperatures (Dijkstra et al., 2013). Others have found that warmer temperatures increase MeHg accumulation, decrease MeHg elimination, and increase oxidative stress (Maulvault et al., 2016; Sampaio et al., 2018), likely because metabolic rates of ectotherms increase with temperature (Sokolova and Lannig, 2008).

Table 2.

The statistical outputs from fitting linear mixed effect models with container as the random effect for the single-factor amphipod experiments (individually examined the effects of organic carbon (here %LOI), temperature (°C), and salinity (ppt)) and for the multi-factor statistical analysis (best fitting model included %LOI, temperature and the interaction of %LOI × temperature) on amphipod BSAF, sediment MeHg (ng/g), and amphipod MeHg (ng/g) for Kittery and Bass Harbor sediments.

Kittery Bass Harbor
BSAF
Factor DF Estimate SE t-value P-value DF Estimate SE t-value P-value
Intercept 9.07 5.23 0.32 16.41 <0.0001 10 −4.28 0.29 16.75 <0.0001
% LOI 8.97 −0.22 0.07 −2.96 0.0161 10 0.55 0.05 −8.5 <0.0001
Intercept 8.16 1.93 0.59 3.30 0.0107 3 0.59 0.77 0.76 0.50
Temperature 8.68 0.09 0.03 3.39 0.0084 3 0.06 0.04 1.77 0.18
Intercept 25.0 4.73 0.15 31.25 <0.0001 4 1.65 0.27 6.11 0.004
Salinity 25.0 −0.02 0.009 −2.8 0.0098 4 0.03 0.01 2.3 0.08
Sediment MeHg
Factor DF Estimate SE t-value P-value DF Estimate SE t-value P-value
Intercept 8.83 −2.07 0.34 −6.03 0.0002 10 −2.99 0.28 −10.71 <0.0001
% LOI 8.75 0.32 0.08 4 0.0033 10 0.34 0.05 6.75 <0.0001
Intercept 7.73 0.03 0.33 0.10 0.92 3 −0.60 0.44 −1.35 0.27
Temperature 8.34 0.007 0.01 0.47 0.65 3 0.02 0.02 0.77 0.50
Intercept 8.74 −0.3 0.2 −1.51 0.17 4 −0.05 0.08 −0.67 0.54
Salinity 9.78 −0.006 0.01 −0.56 0.59 4 −0.02 0.004 −5.85 0.004
Amphipod MeHg
Factor DF Estimate SE t-value P-value DF Estimate SE t-value P-value
Intercept 9.08 4.16 0.17 25.14 <0.0001 2 1.87 0.14 12.93 0.0059
% LOI 9.02 −0.09 0.04 −2.42 0.0388 2 −0.11 0.03 −4.02 0.0568
Intercept 8.23 1.90 0.38 5.05 0.0009 3 −0.01 0.66 −0.02 0.99
Temperature 8.54 0.10 0.02 5.95 0.0003 3 0.08 0.03 2.56 0.08
Intercept 7.44 3.95 0.14 28.43 <0.0001 4 1.60 0.31 5.24 0.0064
Salinity 8.33 −0.01 0.008 −1.5 0.17 4 0.009 0.02 0.58 0.59
Multi-factor
Factor DF Estimate SE t-value P-value DF Estimate SE t-value P-value
Intercept 67.42 6.9 1.13 6.1 <0.0001 44 8.58 1.56 5.5 <0.0001
%LOI 67.16 −0.83 0.22 −3.81 0.0003 44 −0.63 0.21 −2.95 0.005
Temperature 68.79 −0.05 0.05 −0.89 0.38 44 −0.14 0.08 −1.81 0.078
%LOI × Temperature 68.28 0.02 0.01 2.26 0.03 44 0.01 0.01 1.05 0.30
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FIGURE 3.

FIGURE 3.

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Relationships between temperature (°C) and amphipod MeHg (ng/g), sediment MeHg (ng/g), and the biota sediment accumulation factor (BSAF, amphipod MeHg/sediment MeHg). Points represent experimentally observed values and curves represent regression lines fit to log-transformed dependent variables. Red x’s represent points that were removed from analysis due to <50% survival.

Lower %LOI, achieved through the addition of sand to the collected sediment, led to a corresponding reduction in sediment MeHg concentrations (Kittery: r2=0.50, p = 0.0033; Bass Harbor: r2=0.81, p<0.0001; Table 2, Figure 4), but significantly greater MeHg concentrations in amphipods (Kittery: r2=0.29, p =0.039; Bass Harbor: r2=0.79, p = 0.0057; Figure 4). This led to the highest BSAF values at low %LOI for experiments performed using sediment from both locations (Kittery: r2=0.33, p =0.0161; Bass Harbor: r2=0.87, p<0.0001; Table 2, Figure 4). These results agree with previous studies showing that Hg in sediments forms tight bonds with organic matter and therefore reduces the bioavailability of MeHg to invertebrates and fish (Lawrence and Mason, 2001; Mason and Lawrence, 1999; Schartup et al., 2018).

FIGURE 4.

FIGURE 4.

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Relationships between sediment organic carbon (% LOI) and amphipod MeHg (ng/g), sediment MeHg (ng/g), and the biota sediment accumulation factor (BSAF, amphipod MeHg/sediment MeHg). Points represent experimentally observed values and curves represent regression lines fit to log-transformed dependent variables. Red x’s represent points that were removed from analysis due to <50% survival.

In the single-factor experiments, high salinity led to a weakly significant lower amphipod MeHg concentration when organisms were exposed to sediment from Kittery (r2=0.11, p =0.17; Table 2, Figure 5), but no significant effect on the MeHg concentration in organisms exposed to Bass Harbor sediment (r2=0.04, p =0.59; Table 2 Figure 5). The non-significant relationship between sediment MeHg concentration and salinity at Kittery (r2=0.02, p =0.59; Table 2, Figure 5) resulted in BSAF values that decreased significantly with salinity (r2=0.24, p =0.01; Table 2, Figure 5) while the significantly decreasing sediment trend at Bass Harbor (r2=0.69, p = 0.0043; Table 2, Figure 5) led to BSAF values that increased with salinity (r2=0.34, p =0.083; Table 2, Figure 5). Previous studies examining the relationship between salinity and MeHg bioaccumulation have also found contradictory results; some report no significant effect (Reinhart et al., 2018), while others show that lower salinity results in either greater (Fry and Chumchal, 2012; Wang and Wang, 2010) or lower (Dutton and Fisher, 2011) bioaccumulation. At higher salinities the binding of MeHg to Cl− would be expected to increase MeHg uptake (Dutton and Fisher, 2011). On the other hand, Boyd et al., (2017) found that MeHg concentration in sediment was higher at low salinity due to increased microbial methylation in sediments, suggesting that higher salinity limits the ability of sulfate reducing bacteria to methylate Hg. This may have been the mechanism resulting in the negative relationship between MeHg in sediments and salinity exhibited in the Bass Harbor sediments, as differences in sediment concentration of MeHg between treatments would not be anticipated unless microbial activity was affected by the salinity treatment. With regard to site differences, Kittery had on average lower organic carbon concentrations than Bass Harbor, which may result in lower methylation rates (Schartup et al., 2013), although the combined effects of salinity and organic carbon on methylation rates in sediment are not known. Given inconsistent findings on the relationship between salinity and MeHg bioaccumulation in past studies and the difference in effects of salinity on the sediment in this study, further research is warranted on the influence of salinity on MeHg production and its link to bioaccumulation.

FIGURE 5.

FIGURE 5.

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Relationships between salinity and amphipod MeHg (ng/g), sediment MeHg (ng/g), and the biota sediment accumulation factor (BSAF, amphipod MeHg/sediment MeHg). Points represent experimentally observed values and curves represent regression lines fit to log-transformed dependent variables. Red x’s represent points that were removed from analysis due to <50% survival.

3.2. Multi-factor experiments

Multi-factor results give a more nuanced picture than obtained from the single-factor analyses (Table 3; Figure 6). Here significant site-specific responses were detected for temperature (Kittery: p = 0.374; Bass Harbor: p = 0.078 (Tables 2, 3) and no significant effect of salinity was detected for either site. The relation between BSAF and %LOI remains negative (Kittery: p<0.0001, Bass Harbor: p = 0.0046; Table 3), consistent with the single-factor results. However, increased temperature has a negative effect on BSAF at very low %LOI, changing (due to a positive interaction term) to a positive effect at higher %LOI that was significant at Kittery (p = 0.0263) but not at Bass Harbor (p = 0.289; Table 3). As the single-factor temperature experiments were performed at %LOI values at the upper end of each location’s range (being undiluted with sand), they give an incomplete picture of the temperature effect. It appears that when carbon is limiting, higher temperatures limit the bioaccumulation of MeHg, possibly because higher, more stressful temperatures combined with lower food availability in low carbon conditions result in lower food consumption and therefore lower bioaccumulation. Overall, the multi-factor model explains 52% of the variation in BSAF at Kittery and 65% at Bass Harbor.

Table 3.

Results of multi-factor linear regressions of natural log transformed BSAF against environmental variables. Although temperature is not significant for Kittery sediment, it is maintained for consistency with the Bass Harbor sediment and because its interaction term is significant. Salinity was not significant and therefore not included in the model.

Kittery Bass Harbor
Model Term Value P-value Value P-value
Intercept 6.90 < 0.0001 8.58 < 0.0001
% LOI −0.832 0.0002 −0.632 0.0046
Temperature (° C) −0.048 0.374 −0.136 0.078
% LOI × temperature (° C) 0.023 0.0263 0.011 0.289
Marginal R2 0.52 0.65
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FIGURE 6.

FIGURE 6.

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Multi-factor relationships between biota sediment accumulation factor (BSAF, amphipod MeHg/sediment MeHg), sediment organic carbon (% LOI), and temperature (°C) using sediment from Kittery (A) and sediment from Bass Harbor (B). Surfaces represent regression results fit to log-transformed BSAF with salinity held fixed at 20. Black and white triangles represent experimentally observed values above and below the fitted surface, respectively; orange dots on the surface represent the corresponding fitted values. Red lines on the surface represent the sediment organic carbon (% LOI), and temperature (°C) values used in single factor experiments.

3.3. Potential climate change implications

To get a sense of what our experimental results imply for the possible net effect of climate change on MeHg bioaccumulation in L. plumulosus, we estimated the change in BSAF expected to result from a 1.5°C increase in water temperature and a 10% increase in precipitation - realistic projections for the Gulf of Maine by 2100 (Gilbert et al., 2005; Fogarty et al., 2008; Shearman and Lentz, 2010). Using the result of Raymond and Oh (2007), we then estimated that a 10% precipitation increase would translate to a 38% increase in organic carbon availability (see Table S4 for details).

Propagating these changes through our multi-factor model implies that the mean predicted MeHg BSAF in L. plumulosus would decrease from 25 to 13 (~50%) at Kittery and from 12 to 3.5 (~71%) at Bass Harbor, assuming no change in Hg loading. These reductions can be attributed to the presumed increase in sediment organic carbon, which will make MeHg less bioavailable. At these higher carbon levels, the assumed 1.5°C temperature increase can be expected to partially offset the carbon effect by increasing MeHg uptake, possibly via an increase in metabolic rates. Yet, the overall effect is still expected to be a net reduction in the transfer of MeHg from the sediment to L. plumulosus. In fact, even if we assume that wet deposition of Hg, which comprises approximately 30% of Hg loading (Selin and Jacob 2008), would increase proportionally with rainfall increase, our model suggests that mean MeHg concentration in L. plumulosus would still decrease by 48% and 69% at Kittery and Bass Harbor respectively, relative to current values.

Of course, our estimates are rough, as changes in sediment organic carbon will depend strongly on local changes in precipitation, runoff, and other factors, including nutrient loading (Bauer et al., 2013; Howarth et al., 2000; Howarth, 2008; Najjar et al., 2010; Neff et al., 2000). Future levels of Hg loading to estuaries will also depend on local and global policies and trends. Yet, projections from our data-based model suggest that by 2100, climate change may lead to overall lower bioaccumulation of MeHg at the base of the estuarine food chain.

5. Conclusions

While single-factor experiments and data analyses suggested that increased water temperature and lower sediment organic carbon would each individually increase MeHg uptake by the amphipod L. plumulosus multi-factor results were more nuanced. A significant additive interaction between the two factors implied that temperature would only increase MeHg BSAF when sediment carbon concentration was high. The effects of salinity on MeHg uptake were either contradictory by site or insignificant, depending on the data and analysis methods used. The implied net effect of these results along with simple climate projections is that increased precipitation and carbon in the Northeast US may reduce MeHg bioaccumulation by primary consumers. However much more research on this matter is necessary, as few previous experimental studies have simultaneously addressed the effects of these multiple factors on Hg fate in aquatic food webs. In addition to these factors, future experiments should consider the effects of ocean acidification, other potentially interacting contaminants, and transfer to higher trophic levels of the estuarine food web.

Supplementary Material

1

HIGHLIGHTS.

  • Higher temperature and lower organic carbon increased MeHg bioaccumulation

  • Site-specific responses to salinity was observed

  • Multi-factor models showed a significant temperature × carbon interaction

  • MeHg bioaccumulation may decrease due to increased carbon loading

ACKNOWLEDGMENTS

We are very grateful to managing guest editor J. Rinklebe and four anonymous reviewers who provided constructive comments that improved this manuscript. The authors thank Renata Hegyii, Christine Luu, Tammy Hua, Callum Backstrom, and Grace Callahan for experimental assistance. Additionally, we thank Brian Jackson and the Dartmouth Trace Element Analysis laboratory for Hg analysis. Research reported in this publication was supported by the National Institute of Environmental Health Sciences of the National Institutes of Health under Award Numbers P42ES007373 and R01ES021950-01. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Footnotes

Supporting Information

Tables (Table S1, Table S2, Table S3, and Table S4). Table S1 shows the range of MeHg in pre-exposure amphipods raised in Wells sediment across all experiments and replicates. Table S2 shows the range of sediment MeHg before and after the addition of amphipods. Table S3 shows the % survival of amphipods across all treatments. Table S4 describes the assumptions used for the climate change projections.

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