High mercury accumulation in deep-ocean hadal sediments

Ocean sediments are the largest sink for mercury (Hg) sequestration and hence an important part of the global Hg cycle1. Yet accepted global average Hg flux data for deep-ocean sediments (> 200 m depth) are not based on measurements on sediments but are inferred from sinking particulates2. Mercury fluxes have never been reported from the deepest zone, the hadal (> 6 km depth). Here we report the first measurements of Hg fluxes from two hadal trenches (Atacama and Kermadec) and adjacent abyssal areas (2–6 km). Mercury concentrations of up to 400 ng g−1 were the highest recorded in marine sediments remote from anthropogenic or hydrothermal sources. The two trench systems differed significantly in Hg concentrations and fluxes, but hadal and abyssal areas within each system did not. The relatively low recent mean flux at Kermadec was 6–15 times higher than the inferred deep-ocean average1,3, while the median flux across all cores was 22–56 times higher. Thus, some hadal and abyssal sediments are Hg accumulation hot-spots. The hadal zone comprises only ~ 1% of the deep-ocean area, yet a preliminary estimate based on sediment Hg and particulate organic carbon (POC) fluxes suggests total hadal Hg accumulation may be 12–30% of the estimate for the entire deep-ocean. The few abyssal data show equally high Hg fluxes near trench systems. These results highlight a need for further research into deep-ocean Hg fluxes to better constrain global Hg models.

www.nature.com/scientificreports/ may be the largest oceanic Hg sink, there is a critical need to verify the inferred accumulation estimates with data based on sediment sampling.
Here we report Hg concentration and flux data from 12 sediment cores from two hadal subduction trenches, and adjacent abyssal plains and slope, in the Pacific Ocean (Atacama Trench, N = 9 sites, off Chile; Kermadec Trench, N = 3, near New Zealand; Fig. 1 and Table S1). There are 47 subduction trenches, troughs and trench faults in the world's hadal zone, concentrated mainly in the Pacific 24 . Together, the Atacama and Kermadec trench systems represent 2.2% of the total hadal area of about 3.44 × 10 6 km 2 10,24 . Because they are the deepest parts of the ocean basin, trenches are natural accumulators of the organic and inorganic matter that was deposited at the ocean's surface or produced in surface waters 25 . Atacama underlies one of the most productive oceanic regions and has the highest estimated POC flux of any trench (3.2 ± 1.4 g OC m −2 a −1 ), whereas Kermadec has a moderate POC flux (1.6 ± 0.5 g OC m −2 a −1 ) which is similar to the mean of 1.3 ± 0.8 g OC m −2 a −1 across 21 major subduction trenches > 6.5 km deep 26 .

Results and discussion
Sediment dynamics in hadal trenches are governed by two processes: (1) continuous pelagic deposition and (2) infrequent mass wasting/deposition events that translocate large quantities of sediment from the trench slope to the trench interior (typically driven by seismic activity 27,28 ). The profiles of sediment core excess 210 Pb ( 210 Pb ex : defined as the 210 Pb fraction in secular disequilibrium from 226 Ra daughters derived from the atmosphere and the water column) have clear indications of both processes (Fig. S1). Periods of monotonic exponential decreases of 210 Pb ex shown in most core sections reflect relatively constant sediment deposition. Sections of some Atacama cores (At 2, 3, 5, 7, 9 and 10) exhibit short-term 210 Pb ex trend reversals and plateaus that reflect dilution of 210 Pb ex by episodic mass deposition of low 210 Pb ex sediment. We calculated constant linear sedimentation rates (i.e., the sedimentation rates were unvarying down-core) from the periods of continuous deposition, excluding mass deposition events, and thereby provide a conservative estimate of overall sediment deposition rates at the trench axis. The Atacama cores exhibiting mass deposition events have similar calculated sedimentation rates to the other Atacama sites (Table S1).
For our purposes, we grouped Hg concentration data from the top 5-6 cm (4-5 slices; Fig. S2) of each core, where 210 Pb ex was present, as "recent" sediments which, based on the vertical accretion rates, represent material accumulated over about the last 60-190 years (median 120 years). The bottom five slices of each core, including sediments from 10 to 40 cm depth where 210 Pb ex was absent (see Fig. S1), were grouped as "historical" sediments. Although the historical samples can not be accurately dated, they occur at core depths well below the point of 210 Pb ex extinction, which would typically place their deposition prior to about the middle of the nineteenth century given 210 Pb's half-life of 22.3 years.
Atacama sediments overall contained significantly higher Hg concentrations (P < 0.001) than Kermadec (Fig. 2). Sites in the trenches at both locations contained similar recent Hg concentrations to sites on the adjacent abyssal plains and slope (i.e., At1, At7, At9, and Kc7; the difference between trench and abyssal sites is non-significant at P > 0.05). Recent Atacama sediments on average had significantly higher Hg concentrations (188 ± 56 ng g −1 ; P < 0.001) than historical sediments (137 ± 51 ng g −1 ). The exception to this pattern was At2, in which recent sediments had lower Hg concentrations (P < 0.01) than historical. Recent Kermadec sediment Hg concentrations averaged across all sites (44 ± 26 ng g −1 ) were not significantly different from historical sediments (41 ± 16 ng g −1 ; P > 0.05), although they were higher at Kc7 (P < 0.001).
The recent and historical Hg concentrations at Atacama were markedly higher than those in surface sediments in other oceanic regions remote from anthropogenic or hydrothermal sources, where Hg concentrations were usually < 80 ng g −1 9,15 . They were also higher than in other hadal and abyssal sites where mean concentrations ranged from 12 ± 6 to 132 ± 20 ng g −1 (Fig. 3A) 16,18,19 . The mean Atacama values were even higher than in some regions affected by anthropogenic activities. For example, the most contaminated deep-ocean site in the Mediterranean Basin exhibited a mean Hg concentration of 77 ng g − 1 13 . Maximum concentrations in recent Atacama sediments, which ranged up to 401 ng g −1 (see Fig. S2) are the highest reported from remote locations anywhere including in the Kamchatka Trench and abyssal plains (158 ng g −1 16 ) and bathyal areas of the Southern Ocean (87 ng g − 1 15 ). They approach the maxima reported from some of the most contaminated shelf sites world-wide including the Bohai Sea, China (574 ng g −129 ) and the Laurentian Trough, Canada (520 ng g −1 11 ).
POM scavenging and sedimentation of Hg from the euphotic zone, which is ultimately sourced from atmospheric deposition, is likely the main source of Hg in deep-ocean sediments. This is evidenced by Hg isotope analyses of hadal sediments 18 , ocean Hg-primary productivity modeling 3 , and geochemical associations between Hg and POM especially diatoms in particle traps and sediments 15,17,22 . An analysis of the few Hg concentration and flux data available for hadal and abyssal sediments showed positive though non-significant correlations between estimated POC flux and sediment Hg concentrations and fluxes (Fig. 3) which are also suggestive of an upper-ocean source of POM-associated Hg.
There are two other possible sources or processes that can contribute to high Hg concentrations in deepocean sediments. First, post-depositional redistribution of Hg could occur following the decomposition of Hgcontaining POM, releasing dissolved Hg to porewater. Its subsequent diffusion and adsorption onto authigenic Fe and Mn hydroxides in oxic surface sediments can result in Hg enrichment 9,12 . Diagenetic redistribution of Hg is typically negligible in lake and coastal sediments 11,30 , but is less studied and could be important in ocean basins due to different sedimentation and mixing regimes 12,13 . As porewater Hg concentrations were not measured in this study, we cannot directly estimate the magnitude of redistribution. Significant correlations between concentrations of solid phase Hg and reactive Fe (see Fig. S3), an association suggestive of Hg redistribution 12 , were observed in four of nine Atacama cores (At1, At5, At7, At9; Table S2). To test the effect of possible redistribution, we compared mean recent Hg concentrations with those in the whole cores. Whole core data represent the  . Higher Hg values in recent Atacama sediments but not in Kermadec could also be the result of elevated deposition of anthropogenic atmospheric Hg into the eastern Pacific Ocean, compared to lower levels of anthropogenic Hg in ocean waters near Kermadec 3 . While we cannot resolve the two alternate explanations, the absence of significant Hg-reactive Fe correlations at the majority of Atacama sites, and the small increase in recent Hg concentrations relative to whole cores at both trenches, suggests that any effect of redistribution on recent sediment Hg concentrations and fluxes was small. A second possible Hg source in deep-ocean sediments is seafloor hydrothermal vents associated with midocean ridges. Globally, vents are thought to contribute minor amounts of Hg to oceans, ≤ 100 t a −1 1,22 , but could be locally important. The Atacama study area is several thousand km east of the nearest known hydrothermal field 31 indicating that, in this area with the highest Hg concentrations, hydrothermal influences are negligible. The Kermadec trench is located relatively close to a hydrothermal field 31 , but no studies have been conducted on vent releases or seawater Hg concentrations in this region. However, there is little evidence of significant hydrothermal impacts on Hg concentrations in seawater [32][33][34] or biota 18 in the vicinity of vent plumes elsewhere, suggesting that the possibility is unlikely in this study. Overall, therefore, the Hg concentrations in these trench sediments are likely to predominantly reflect POM-associated transport of Hg from the euphotic zone.
Mean total Hg fluxes in recent sediments at Atacama (63.6 ± 30.8 µg m −2 a −1 ) were significantly higher (P < 0.001) than in historical sediments (44.4 ± 19.5 µg m −2 a −1 ), and also significantly higher (P < 0.001) than recent Kermadec sediments (10.4 ± 7.5 µg m −2 a −1 ; see Fig. 2B). There was no significant difference between average fluxes measured in trenches and in abyssal plain and slope sites at either location (P > 0.10). www.nature.com/scientificreports/ To place these results in context, the relatively low recent Hg flux measured at Kermadec (10.4 µg m −2 a −1 ) is 6-15 times higher than the currently estimated deep-ocean average of 0.7-1.8 µg m −2 a −1 1,3 . Because the POC flux at Kermadec is similar to the average of all of the world's trenches > 6.5 km depth 26 , Kermadec may approximate the global average Hg flux in the hadal. The median recent flux across our study sites (39.1 µg m −2 a −1 ) was 22-56 times larger than the inferred deep-ocean average Hg flux, but the median includes Atacama with the highest POC flux in the world, and which therefore may have a substantially higher Hg flux than most other trenches. Overall, however, these results indicate that some hadal trenches and adjacent abyssal areas are intense focal points of Hg accumulation. The question arises as to what impact these high hadal fluxes might have on global deep-ocean Hg accumulation rates.
To tentatively calculate the total hadal zone Hg flux, the few available data from hadal and abyssal sites (the present study, and Aksentov and Sattarova 17 ) were used to approximate Hg fluxes for each trench system using the much larger global trench POC database. Individual trench estimates were summed to arrive at a total hadal Hg accumulation rate. POC flux data are available for 18 of the deepest trenches > 6.5 km depth, including Atacama and Kermadec 24,35 , representing 92% of the global hadal area below 6.5 km. Applying a Hg:POC regression slope (± standard error, SE) of 16.1 ± 2.9 μg Hg g POC −1 (see Fig. 3B), we arrive at a preliminary estimate of total Hg burial of 16.9 ± 1.0 t a -1 in this zone (see Table S3). Scaling up to the much larger hadal area bounded by the 6 km isobath 10 , the total Hg flux is estimated to be 73 ± 4.4 t a -1 . The error terms for the 18 trenches and for the total hadal zone were propagated from the SE of the Hg:POC regression slope applied to each trench's POC data. We emphasize the uncertainty associated with the 73 t a −1 value because of the few hadal or abyssal sites in total that have been sampled for Hg fluxes (N = 3), the large variation in fluxes between cores within the study trenches, and the relatively large confidence intervals associated with the Hg:POC regression (see Fig. 3B).

Conclusions
This study has substantially expanded the knowledge base concerning Hg flux in the deep-ocean. These results increase by six-fold the number of dated cores analyzed from this zone and provide the first estimates of hadal Hg flux, which is shown to be high at both study sites relative to the currently accepted deep-ocean average flux. Although still limited in number and geographical scope, the results can be placed in the context of the current estimate of deep-ocean Hg accumulation. Our first order estimate of 73 t a −1 for hadal Hg burial represents  www.nature.com/scientificreports/ 12-30% of the putative deep-ocean accumulation of 240-600 t a −1 1,3 , occurring within an area equal to 1.1% of the total deep-ocean. This estimate omits Hg flux in the much larger abyssal zone which is 85% of total ocean area 10 . Given the evidence of similarly high Hg fluxes in some abyssal sediments (this study and Ref. 17 ), and even higher fluxes in high productivity bathyal areas of the Great Southern Ocean 15 , it is possible that the total deep-ocean Hg accumulation is higher than is presently believed. Our results thus call for extensive additional sampling of the deep-ocean to better constrain these preliminary estimates and to improve global Hg modeling.

Methods
Sampling. Sediment was for most part recovered by a multi-corer 36 , but in some cases we were successful using box coring (site Kc7) or an autonomous lander system for core recovery (Kc4). Recovered sediment cores were transferred to an onboard laboratory that maintained in situ bottom water temperature (2-4 °C). For the Kermadec Trench system, sediment cores were sectioned in 1 cm slices down to 2 cm depth, 2 cm slices to 10 cm and subsequently in 5 cm slices to the core bottom. For the Atacama Trench system, the cores were sectioned in 1 cm slices down to 10 cm, 2.5 cm slices to 20 cm, followed by 5 cm slices until the bottom of the core. Samples were homogenized in plastic bags and stored at -20 °C until laboratory analysis onshore. Pb ex activity (Bq g −1 ) in the core sections displaying exponential decreases in the plots. Instead of the core depth (cm), cumulative mass depth (g cm −2 ) obtained from the core depth and the dry bulk density (g cm −3 ) was used to express the sediment accumulation rate (initially as g cm −2 a −1 ).
Hg analysis. Mercury in the sediment samples was determined as total Hg on a Hydra IIC direct mercury analyzer (Teledyne Leeman Labs, Hudson, NH, USA) using thermal decomposition, amalgamation and atomic absorption spectrophotometry following EPA Method 7473 42 . 10-50 mg of individual freeze-dried sediment samples were weighed into quartz boats. Mercury concentrations were quantified by the external standard method with calibration curves ranging from 1 to 1500 μg g −1 . Within every batch of 10 samples, 3 blanks, 1-2 pairs of duplicates and 2-3 certified reference materials (CRMs: MESS-3, DOLT-5; and NIST 2709a and PACS-3, obtained from the National Research Council of Canada and NIST, respectively) were analyzed. In order to be deemed valid, the CRMs must fall within the range of the certified mean ± standard deviation. If CRM concentrations were outside the acceptable range, 2 more CRMs were analyzed. If the following CRMs were still outside the acceptable range, the instrument was re-calibrated. The mean CRM recoveries were 101.9 ± 9.0% and were within the expected ranges.
Reactive Fe analysis. Two reactive Fe extraction procedures were employed on frozen sediments-Fe-DCA (Fe species solubilized in a dithionite-citrate-acetic acid solution (50 mg mL −1 sodium dithionite in 0.35 M sodium citrate, 0.2 M acetic acid, pH 4.8 for 1 h)), and Fe-HCl (Fe species solubilized by a mild HCl extraction (0.5 M HCl for 1 h)). Fe-DCA extracts the non-silicate-bound Fe fraction (oxides and authigenic Fe(II) phases excluding pyrite), whereas Fe-HCl releases poorly crystalline oxides and authigenic Fe(II) but also leaches some Fe from silicates 43,44 . Fe in the extract solutions was determined as total Fe using Ferrozine 45 . Concentrations were calculated on a dry weight basis using the water content.
Statistics. Concentration and flux data in the text are represented as mean ± standard deviation (SD) values.
Mercury concentration and flux data were not normally distributed in some cores, and differences between recent and historical sediments in these cases were tested with a Mann-Whitney Rank sum test. Those with data that were normally distributed and which satisfied the assumption of equal variance were analysed with t-tests. Linear regressions analysed relationships between mean Hg concentrations and fluxes and POC fluxes because the combined data were normally distributed. We used SigmaPlot 14.0 Software (Systat Software Inc.). Error propagation was calculated with the online calculator at www. julia nibus. de.

Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.