Legacy groundwater pollution as a source of mercury enrichment in marine food web, Haifa Bay, Israel

Journal Pre-proof Legacy groundwater pollution as a source of mercury enrichment in marine food web, Haifa Bay, Israel

E. Shoham-Frider, Y. Gertner, T. Guy-Haim, B. Herut, N. Kress, E. Shefer, J. Silverman PII:

S0048-9697(20)30221-7

DOI:

https://doi.org/10.1016/j.scitotenv.2020.136711

Reference:

STOTEN 136711

To appear in:

Science of the Total Environment

Received date:

23 September 2019

Revised date:

13 January 2020

Accepted date:

13 January 2020

Please cite this article as: E. Shoham-Frider, Y. Gertner, T. Guy-Haim, et al., Legacy groundwater pollution as a source of mercury enrichment in marine food web, Haifa Bay, Israel, Science of the Total Environment (2020), https://doi.org/10.1016/ j.scitotenv.2020.136711

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© 2020 Published by Elsevier.

Journal Pre-proof

Legacy groundwater pollution as a source of mercury enrichment in marine food web, Haifa Bay, Israel

Shoham-Frider E.1*, Gertner Y.1, Guy-Haim T.1, Herut B.1, Kress N.1, Shefer E.1 and Silverman J.1

Israel Oceanographic and Limnological Research, Haifa 31080, Israel

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* Corresponding Author: [email protected]

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1. Introduction

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The Minamata environmental disaster in Japan (Fujiki and Tajima, 1992) raised global awareness of mercury, as a toxic and hazardous pollutant for humans, originating primarily

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from consumption of fish contaminated with methylmercury (MeHg) (Hammerschmidt and

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Fitzgerald, 2006). Specific guidelines for mercury concentrations in fish, and fish consumption restrictions, especially for pregnant women, exist nowadays in most developed countries (for example

https://www.fda.gov/Food/FoodborneIllnessContaminants/Metals/ucm393070.htm, accessed 18 December 2019). MeHg, one of the most toxic compounds of Hg, has an assimilation efficiency four times higher than inorganic Hg (Mason et al., 1996) and bioaccumulates and biomagnifies in marine food webs. As a result, the proportion of MeHg increases up the marine food chain and constitutes more than 90% of THg in fish (Gosnell and Mason, 2015; Mason et al., 2012; Mason et al., 1996; Morel et al., 1998) . The main source of Hg to the oceanic food web is considered to be atmospheric (e.g. Fitzgerald et al., 2007; Mason and Sheu, 2002). However, land based point sources, resuspension of Hg contaminated Page 1 of 34

Journal Pre-proof sediments, and Hg pollution in submarine groundwater discharge are also important sources of Hg to the coastal biota (e.g. Bone et al., 2007; Harada, 1995; Rudd et al., 2018; Shefer et al., 2015).

Haifa Bay (HB, hereafter), located along the northern Mediterranean shore of Israel (Fig. 1), has been a local hot spot for heavy metals pollution since the early half of the 20th century, following port development, rapid urbanization, and industrialization of the region

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(e.g. Hornung et al., 1989; Hornung et al., 1984; Kronfeld and Navrot, 1975). During 1956–

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1976, ca. 22 tons of inorganic Hg were discharged at the shoreline into HB from a chlor-

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alkali plant (Electro-Chemical Industries LTD; ECI henceforth), located south of the city of

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Akko (Fig. 1). Signs of this pollution and its impact on THg concentrations in the biota of HB were documented and reported numerous times in the scientific literature since the

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1980s (Herut et al., 1997; Herut et al., 1996; Hornung and Kress, 1991; Hornung et al.,

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1989; Hornung et al., 1984; Krom et al., 1990; Shefer et al., 2015). As a result, Israeli authorities imposed a pre-treatment of the ECI effluents that reduced the Hg loads to 74, 64,

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and 34 kg·y-1 in 1992, 1997, and 1998, respectively. During 1999-2003, the loads from this source were further reduced from 6 to less than 1 kg·y-1 (Malester and Marek, 2006). Eventually, the plant was shut down and abandoned in 2003, in the wake of a fire that destroyed its manufacturing facilities. However, not all of the hazardous waste was removed from the plant and large amounts of elemental Hg were left in plain sight, while some may have been buried at different locations in the area of the plant prior to its dereliction (Fig. S1). The second major source of Hg pollution in HB is the Qishon River that received until the early 2000’s effluents from chemical and petrochemical industries, polluted urban and agricultural runoff, as well as effluents from the Haifa Municipality domestic sewage

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Journal Pre-proof treatment plant (Cohen et al., 1993). The estuary of the river is located at the eastern end of Haifa port and is open to southern HB. The port acts as a trap for much of the contaminated sediments and organic matter originating from the Qishon River (Arenas et al., 2012). However, during significant rain events, flooding in the Qishon River can transport substantial amounts of contaminated sediments and organic matter further into HB (Op. Cit.). Regardless, some of the highest concentrations of THg in bottom sediments are found in Haifa Port even today, nearly 2 decades after Hg loading from the Qishon industries was

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prohibited (Bareket et al., 2016; Shoham-Frider et al., 2012). Haifa Port and the Qishon

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River have undergone massive development, expansion and dredging operations, since the

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early 2000s causing widespread resuspension of contaminated sediments (Shefer et al.,

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2015).

Hg contaminated fish, benthic fauna, macro-algae and sediments from HB were recorded as

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early as 1972 (Hornung and Kress, 1991; Yannai and Sachs, 1978). Since 1981, THg

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concentrations in sediments and biota have been monitored regularly by the Israel Oceanographic and Limnological Research institute (IOLR), as part of Israel’s National

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Monitoring Program in adherence with the Barcelona Convention for the protection of the Mediterranean Sea (https://ec.europa.eu/environment/marine/internationalcooperation/regional-sea-conventions/barcelona-convention/index_en.htm, accessed 18 December 2019). According to these measurements, there was a dramatic decrease of THg burden in marine biota and sediment concentration from the mid-1980s to ~2000, nearly coinciding with decreasing industrial Hg loads into HB (Bareket et al., 2016; Herut and Galil, 2000; Herut et al., 1999; Shefer et al., 2015). Despite these apparent improvements, the THg burden in some biota species was still higher in HB, compared to other areas along the Israeli coast (e.g. Shefer et al., 2015). In addition, during the period of 2006-2014, the THg burden of three commercial fish species (Diplodus sargus, Lithognathus mormyrus,

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Journal Pre-proof Sargocentrum rubrum), collected in the northern part of HB, started to increase, reversing the previous negative trend (Herut et al., 2015). In 2012, the THg burden in ~19% of these species specimens collected from HB exceeded the national guidelines for safe consumption of fish and their products, which are 0.5 mg kg -1 and 1 mg kg -1 (Israeli Ministry of HealthFood & Nutrition Services). In contrast, the THg burden in these species collected in other areas along the Israeli coast as well as other fish species (Siganus rivulatus, Pagellus erythrinus, Mullus barbatus) collected from HB and other areas along the coast, remained

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relatively low and constant. The increase in THg burden of HB fish was unexpected. Since

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2000 essentially no Hg was introduced to HB from terrestrial sources. Therefore, the Israeli

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Ministry of Environmental Protection commissioned a study to identify the source and

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causes of increasing THg burden in HB commercial fish. Based on the facts that Hg burden in fish only from northern HB increased despite the fact that there were no industrial

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emissions and THg concentrations in HB sediments decreased over the same period, we

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hypothesized that Hg polluted groundwater from the vicinity of the ECI is the new and previously unconsidered source of Hg to the Bay. To test this hypothesis, we measured THg

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and MeHg in seawater, coastal groundwater, suspended particulate matter, plankton, macroalgae, benthic fauna and marine and beach sediment samples, and mapped their spatial distribution and bioaccumulation up the food web.

2. Materials and Methods 2.1 Study site Seawater, groundwater, inshore (beach), and marine sediments, suspended particulate matter (SPM), mixed plankton (i.e., phytoplankton and zooplankton), macro-algae, intertidal and subtidal mollusks, and sponges were sampled at different sites in HB and at two stations to the north of the Bay. One area, located south of the bay was designated as the reference site

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Journal Pre-proof (RS) (Fig. 1), which is known to be unpolluted (Herut et al., 2015). The sampling sites and stations, sampling dates, and environmental matrix sampled are detailed in Table 1. The parameters analyzed for each sampling and environmental matrix are detailed in Table S1.

2.2 Sampling and storage Seawater and groundwater: Seawater (2-3L) was sampled using a peristaltic pump (ColeParmer Instrument co., MasterFlex E/S Portable Sampler), or directly from the sea surface.

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Table water samples (groundwater hereafter) (0.5L) were taken by digging 50-120 cm 1-3

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deep pits along 10-30 m from the waterline, cross shore transects along the shore of northern

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HB, until reaching the saturated zone immediately above the water table. Then, a stainless

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steel piezometer was inserted into the pit and hammered until it reached the water table and groundwater was pumped through it using a peristaltic pump into sampling containers.

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Groundwater density (precision of ±0.1 kg m-3) and temperature measurements using an

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Anton-Paar handheld density meter DMA 35 Basic were made onsite and later on converted to salinity using the equation of state for seawater from the 19th edition of standard methods

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(Fofonoff and Millard Jr, 1983).

Water samples for THg analysis were transferred to pre-cleaned new polypropylene sterile tubes containing acidified BrCl (EPA 1631). The dissolved fraction of THg (DTHg) was sampled by filtering the water through a 0.45 µm GFF filter prior to the addition to the BrCl solution. The samples were kept refrigerated in the dark until analysis within 1 week of sampling. Additional seawater and groundwater samples for MeHg determination were transferred to acid pre-washed plastic containers that contained H2SO4 (EPA method 1630), and were shipped refrigerated (4°C) to Brooks Rand laboratories in the USA for analysis. Water for total organic carbon (TOC) analysis, were sampled into HCl pre-washed glass containers, and preserved with 20 µL 32% HCl. For the analysis of suspended particulate

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Journal Pre-proof matter (SPM), 2L of seawater were filtered through pre-weighted 0.45 µm polycarbonate filters (after pre-filtration of 63 µm), which were kept frozen and re-weighted after freezedrying in the lab. Later on, the filters were digested for the analysis of THg analysis in the SPM. Total particulate Hg (PTHg) concentrations in water (ng L-1) was calculated from the THg concentration in SPM and the concentration of SPM in seawater.

Sediments: Marine sediments (upper 2 cm) were sampled by a van-Veen grab with maximal

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volume and penetration depth of 20L and 20cm, respectively. Inshore sediments were

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sampled with a plastic spoon. Sediments were sampled into polypropylene containers and

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frozen. The frozen sediments were lyophilized for 48 hours and then dry sieved through a

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1000 µm sieve to remove the larger, extraneous fraction. Plankton: Plankton samples were collected by towing a Bongo plankton net (Sea-Gear 9600,

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30 cm pairs, USA) with 65 and 200 µm mesh nets to measure THg in the phytoplankton size

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fraction (>65 µm) and meso-zooplankton size fraction (>200 µm) (Caspers, 1980; Hasle and Sournia, 1978). Three tows of 20 minutes each, at 3 knots were conducted at each location

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during the daytime on different occasions (Table 1, Fig. 1). The collected material was removed from the nets, vacuum filtered onto a 0.7 µm GFF or 0.45 µm polycarbonate filters, frozen and lyophilized for 48 hours. The dry planktonic matter was removed from the filter, ground, homogenized and kept in sealed new polypropylene tubes. The collected material was analyzed as total mixed plankton without species identification (Back et al., 2003; Guedes Seixas et al., 2014). Benthic organisms: Specimens of benthic macroalgae, mollusks and sponges were collected by SCUBA divers from the submerged calcareous Kurkar ridges (water depth of 10-12 m), and from intertidal beach-rocks. Four species of macro-algae were collected: Galaxaura rugosa at Akko and the reference site (RS); Ulva sp. at Achziv (ACH) and Akko; Palisada

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Journal Pre-proof perforata (formerly Laurencia papillosa) and Jania rubens, both at ACH and RS. The algae from each site were divided into replicate samples, freeze-dried and ground to a homogenized powder. The gastropod Cerithium scabridum was sampled at Shavey- Zion (SZ) and at RS, ca. 20-30 specimens from each site. Since the soft tissue of C. scabridum could not be efficiently separated from the shell, after lyophilization the mollusks were ground to a powder with their shells. Specimens of the bivalve Spondylus spinosus were collected from the Kurkar ridges in HB and RS. The specimens were measured (total

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weight, shell length and width) and the soft tissue of each specimen was removed, weighed,

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freeze-dried, ground and kept in sealed new polypropylene tubes. Specimens of two species

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of long-living sponges: Crambe crambe and Ircinia variabilis, were collected from the

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Kurkar ridges (~12 m depth) near SZ, Akko, South HB and RS. C. crambe creates colonies in the form of thin orange-red plates coating rock surfaces, thus cannot be referred to as

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individual specimens. Hence, at each site, the hard substrates covered with C. crambe were

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removed entirely, and brought to the lab, where the sponge was scraped off the substrate, and composited to one representative sample for each station. I. variabilis that grows in a

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defined form of elastic and massive tubes could be analyzed individually. Finally, specimens of the limpet Patella sp. were manually collected from the intertidal in Haifa Port and at Akko, SZ, ACH and RS. In the lab, all benthic samples were kept frozen in plastic containers with seawater. After sorting, identification of species and measurement, the soft tissue was freeze –dried, ground, homogenized and stored in dark sealed glass jars.

2.3 Analytical methods Total mercury: THg in groundwater and seawater was measured following oxidation by bromine monochloride (US EPA Method 1631) and analyses by cold vapor atomic fluorescence spectrometry (CVAFS), with a Merlin Millenium system (PS Analytical, UK)

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Journal Pre-proof after SnCl2 reduction and purging with high purity argon (Shoham-Frider et al., 2007). The method detection limit was 3 ng L-1. Samples for the analysis of THg in SPM, sediments and biota, were digested with concentrated HNO3 in Teflon lined, high-pressure decomposition vessels (Hornung et al., 1989; Shoham-Frider et al., 2002; Shoham-Frider et al., 2009). Biota and sediment samples were digested in duplicates, unless there was not enough available material. Hg analyses were performed by CVAFS with a Merlin Millenium system. Method detection limits for SPM, sediment and biota samples were 0.07

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ng g-1 dry wt.

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Methyl mercury: MeHg in groundwater and seawater was measured by distillation, aqueous

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ethylation, purge and trap, desorption, and CVAFS (analyzed at Brooks-Rand laboratories

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USA according EPA-1630 method), with a method detection and reporting limits of 0.004 and 0.015 ng L-1, respectively. MeHg was extracted from sediment samples with

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dichloromethane as a halide salt followed by a back extraction into an aqueous phase,

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separated, oxidized by BrCl and measured as THg (Cai et al., 1997; Longbottom et al., 1973; Sakamoto et al., 1992). While the procedure extracts both methyl- and ethyl-Hg, it

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was assumed that all extracted organic Hg was present as MeHg, as determined previously in samples from the study region (Shoham-Frider et al., 2007) and elsewhere (Cai et al., 1997; Hintelmann and Wilken, 1993; Wu, 1991). MeHg was extracted from biota samples by acid leaching followed by toluene extraction and back extraction with sodium thiosulfate (Azemard and Vassileva, 2015). The MeHg in the final aqueous solution was oxidized to THg with acidified BrCl, and measured by CVAFS. The method for this last stage was developed and validated inhouse (Shoham-Frider et al., 2007) THg and MeHg concentrations in sediments and biota are expressed as ng g-1 dry weight. For text simplicity, dry weight will not be added to the units hereafter.

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Journal Pre-proof Total organic carbon: TOC in water was measured by high temperature combustion and IR detection of the CO2 produced during combustion with a Shimadzu TOC VCPH. TOC in sediments was determined by potentiometric titration after digestion with potassium dichromate (Gaudette et al., 1974; Leong and Tanner, 1999). Quality control and quality assurance for THg determination was performed with the following international certified reference materials (CRM): DORM4, DOLT5, IAEA-407, NIST 2781, NRCC-MESS-2 and IAEA-405. The CRMs were treated and analyzed in the

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same manner as the samples in each analytical run. All results were within 10% of the

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certified values. The method for MeHg determination was validated using International

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certified reference materials (fish products from NRC-CNRC and IAEA) which contained

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MeHg. The recovery percentages of MeHg using this method were 90% (n=16), 100.3%

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(n=9) and 96.8% (n=4), for DORM4, DOLT5 and IAEA-407, respectively.

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Statistical analyses were performed with XLSTAT (Addinsoft TM, version 2013.6.01) with a significance level of α=0.05. Differences between data groups were tested for significance

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using the non-parametric Mann–Whitney test and the correlations’ significance were tested by Pearson’s test.

3. Results

3.1 Seawater THg in seawater was measured during four surveys, with different results (Table S2b). On February 2015, THg in seawater was below the level of quantification (<3 ng L-1) except at Akko marina (FM1) where the concentrations were 176 and 17 ng L -1 at the surface and bottom, respectively. In May 2015, THg was detected in seawater samples taken from the surf zone (ca. 80 cm water depth) across from stations FM4 (within the ECI) and FM35 (ca. Page 9 of 34

Journal Pre-proof 1000 m north of the ECI), concentrations of 7.6 and 9.7 ng L-1, respectively), while on July 2015 THg concentrations across from Akko’s bathing beaches (stations FM36-FM43) were <3 ng L-1. In April 2016, the THg concentrations in seawater sampled in the surf zone across from stations FM3 and FM32 were 4.3 and 17.8 ng L-1, respectively. In the surf zone along the Akko bathing beaches further north, the concentrations across from stations FM37, FM38 and FM40 were 31±7 (n=4), 40±7 (n=4), and 19±11 (n=4) ng L -1, respectively. These results indicate potential seasonality, where concentrations of THg in shore waters are

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higher in spring (April-May) compared to summer.

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THg concentrations in SPM ranged from 110 to 878 ng g-1. At the Akko marina (FM1), and

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the surface and near the bottom and the surface waters at the western Haifa Port (FM7), THg

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concentrations were highest 721- 878 ng g-1 (Table S2a). The PTHg concentrations in seawater at the RS were the lowest calculated (0.28 and 0.55 ng L-1, surface and near bottom

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samples, respectively), and highest at the Akko marina (7.1 and 9.7 ng L-1, near bottom and

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surface samples, respectively) (Table S2). At the other stations, the PTHg ranged from 0.8 and 5.7 ng L-1. As expected, comparison of SPM and PTHg concentrations yielded a good

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correlation (r2=0.91, P<0.0001).

MeHg concentration in surf zone seawater across from stations FM4 (within the ECI) and FM35 (ca. 1000 m north of the ECI) in May 2015, was 0.02 ng L -1 that constituted 0.21 and 0.26%, respectively, of the THg concentrations measured at these stations. TOC concentrations in seawater ranged from 0.83 to 1.51 mg L-1 (Table S2). The highest concentrations were found inside and near the Akko marina (FM1 and FM2) and at the entrance to the fishing harbor (FM8) (1.29±0.14 mg L-1, n=6), while at the RS the mean concentration was 0.95±0.16 mg L-1 (n=2) (Table S2).

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Journal Pre-proof SPM concentrations at the RS were 0.7 and 1.7 mg L-1 at the surface and bottom, respectively, while in all HB stations the concentrations varied from 2.4 to 12.6 mg L-1. The highest concentrations of 11.0 and 12.6 mg L-1 were measured at the surface inside Akko marina (FM1) and entrance to the fishing harbor (FM8), respectively.

3.2 Groundwater Very high THg concentrations (13160 and 28140 ng L-1) were measured in unfiltered

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samples taken from the groundwater at sites along the ECI beach in February 2015 (Table

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S3). In May and July 2015, THg concentrations in unfiltered groundwater sampled at

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stations along the ECI beach (FM3, FM4, FM31-FM33) ranged widely, from 22.4 to 6381

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ng L-1, with two extreme values of 55628 and 251216 ng L-1 at stations FM3c and FM32c, respectively. THg concentrations decreased southwards and northwards of the ECI beach

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and towards the sea with increasing salinity in most cases, varying between 7 and 751 ng L-1

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(Fig. 2) (Table S3). In April 2016, THg was measured both in unfiltered and filtered groundwater, and in unfiltered seawater from the surf zone (Tables S2b and S3).

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Concentrations of THg in unfiltered groundwater were very heterogeneous both within stations and between stations (1328 ± 1712 and 2831 ± 2150 ng L-1, at FM32 and FM3, respectively), while DTHg concentrations were lower and homogenous (19 ± 1 and 72 ± 16 ng L-1, at FM32 and FM3, respectively). It is likely that the heterogeneity of THg concentrations in unfiltered groundwater resulted from the presence of Hg enriched particles. At the same time, THg concentrations in seawater across from stations FM3 and FM32 (18 ± 2 and 4 ± 0.1 ng L-1, respectively) were correlated only with the dissolved fraction of THg in groundwater (n=4, r2=0.986, p=0.007). MeHg in groundwater, as for seawater, was measured only once in May 2015. The concentrations ranged from 0.08 to 1.91 ng L-1, except at station FM32-c where MeHg was

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Journal Pre-proof 57.9 ng L-1 (Table S3). At this station THg was the highest (251,216 ng L-1), probably due to the presence of Hg-enriched particles, as noted above, but the fraction of MeHg from THg was low (0.02%), despite its high concentration. The MeHg concentration in seawater sampled from the surf zone across from stations FM4 and FM35 was 0.020 ng L-1, which constituted 0.24% of corresponding THg concentrations.

3.3 Marine and Inshore Sediments

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THg in the marine sediments of HB and semi-enclosed sites ranged from 86 to 523 ng g-1

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(Table S2). The highest concentration was found in sediments from Akko Marina (FM1)

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followed by western Haifa Port (FM7). THg in inshore sediments was highest opposite the

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ECI (2201 and 1092 ng g-1, stations FM3 and FM32, respectively), and decreased southwards and northwards to 308 and 209 ng g-1, respectively and towards the shore (Fig.

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2, Table S3). THg in the sands of Akko’s bathing beaches, up to 2.5 km north of the ECI

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(Fig. 1, FM37-38, FM40), were similar in the summer (160-180 ng g-1, August 2015) and similar but slightly higher in the spring ( 216-229 ng g-1 , April 2016). The THg

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concentration at the RS was much lower, only 2 ng g-1, and similar to the concentrations found at other stations along the Mediterranean coast of Israel (Herut et al., 2015). MeHg was not detected in sediments from nearshore stations in Haifa Bay, while at the Akko marina and the Haifa and Qishon ports (FM1, FM7, FM8), MeHg concentrations ranged from 0.87 to 3.35 ng g-1, with MeHg/THg of 0.5% - 0.9% (Table S2). At these stations a significant positive correlation was found between MeHg and THg (r2=0.82, p=0.03, n=5). MeHg in the inshore sediments was lower (0.18-0.87 ng g-1) with MeHg/THg of only 0.05-0.08% (Table S3) and no statistically significant correlation between them. TOC concentrations in the sediments were typically low at the RS (0.06%), higher but still low in nearshore sediments of HB (0.15±0.01% at stations FM2, FM5), and higher at the

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Journal Pre-proof semi-enclosed sites of Akko marina (FM1), Haifa Port (FM6, FM7) and the Qishon Port (FM8), where TOC was 1.23 ± 0.44 % (Table S2). The inshore sediments that were sampled in the area of the ECI had low TOC concentrations (0.04-0.08% and are not presented in Table S2).

3.4 Biota The THg and MeHg concentrations measured in specimens from four taxonomic groups

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(plankton, macroalgae, mollusks and sponges) from different sampling sites (Fig. 1, Table

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1a) are detailed in Table S4.

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Plankton: THg in plankton (>65 µm) ranged from 25.4 to 140 ng g-1. There were significant

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differences among regions but not between sampling dates (Table S4). When the samples were pooled by sampling areas, THg was significantly higher (p<0.0005) in plankton from

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SZ and northern HB (n=10, 113±30 ng g-1) compared to the samples from central HB and

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RS (n=10, 47.5±15 ng g-1; Fig. 3). In the >200 µm fraction, the concentration of THg ranged from 24.3 to 119 ng g-1 with higher concentrations, but not statistically significant (maybe

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due to the small sample size) in July 2016 compared to April 2016, and in SZ and Akko compared to RS. However, while there were no significant differences between THg concentrations measured in corresponding plankton samples of >65 µm and >200 µm, there was a significant positive correlation between them in all measurements (n=14, r2=0.654, P<0.0005). Macroalgae: THg concentrations in benthic calcareous macroalga G. rugosa collected in northern HB, near Akko, were 5-6 times higher than in those collected at the RS (18.4 and 3.3 ng g-1, respectively). MeHg, which was not detected in the specimens from RS, constituted more than 30% of THg in the algae collected in northern HB. Ulva sp., collected from northern HB and ACH had similar THg concentrations (136 and 105 ng g-1,

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Journal Pre-proof respectively). MeHg, which was not detected in the specimens from ACH, constituted 3.4% of THg in specimens from northern HB. P. perforata and J. rubens collected in ACH exhibited higher THg than the specimens collected at RS, however MeHg was not detected in all samples. MeHg was detected only in specimens collected in northern HB. Mollusks: THg in samples of the gastropod C. scabridum, from SZ and RS were 14.4 and 4.4 ng g-1, respectively. The THg concentrations were measured in the oyster S. spinosus twice in this study, March 2015 and July 2016. No significant differences were found

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between the sampling dates, therefore, the data was pooled by sampling site (SZ, northern

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HB, southern HB and RS). (Table S4, Fig. 3). THg concentrations ranged from 135 to 282

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ng g-1. The concentrations were similar in specimens from SZ, northern and southern HB,

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and were all significantly higher (p=0.001) than the concentrations measured in specimens from RS. In contrast, the MeHg concentrations that ranged from 9.7 to 22.7 ng g-1, were

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similar in specimens from SZ and northern HB, that were significantly higher (P<0.0001)

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than the concentrations measured in specimens collected in southern HB and RS. The relative contribution of MeHg to the THg was also higher in specimens from SZ and

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northern HB (Table S4). No correlation was found between THg and MeHg concentrations, at any of the sites.

The limpet Patella sp. was sampled twice from intertidal beach rocks in ACH, Akko, QY, Haifa Port and RS. THg concentrations ranged from 52.4 to 209 ng g-1 (Table S4). Samples from QY exhibited higher concentrations in December 2015 (winter) compared to May 2016 (spring). In May, THg concentrations were significantly higher in specimens from Akko, compared to every other site sampled. There was no difference in THg concentrations between specimens from ACH and RS. Comparison of THg to shell size yielded a weak, but significant negative correlation (n=35, r2=0.20, p=0.007) only in the specimens from Haifa Port. MeHg in Patella sp. ranged from 3.96 to 25.2 ng g-1 and it constituted 4.2 to 20.8 % of

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Journal Pre-proof the THg. No correlation was found between MeHg concentrations and shell size and it was higher in specimens from Akko, compared to the other sites. However, there was a positive correlation between THg and MeHg concentrations in all specimens of Patella sp. (r2 = 0.59, n = 18, p <0.0005). Sponges: In the sponge C. crambe, which is known to filter-feed on microorganisms from the water column, THg concentrations were highest in SZ (269 ng g-1) and were significantly lower in northern and southern HB, where the concentrations were similar (41

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and 40 ng g-1, respectively) (Table S4). At RS, the THg concentration in sponge specimens

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was lower, 21 ng g-1. In the sponge I. variabilis, no differences were found in THg

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concentrations between specimens sampled at SZ and northern HB (THg = 418±124 ng g-1),

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however, they were higher (p<0.0005) than those measured in specimens from southern HB and RS, which were also similar to each other (THg = 200± 68 ng g-1). MeHg

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concentrations were 15±4.7 ng g-1 in specimens from SZ and Akko, and <0.01 ng g-1 in

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4. Discussion

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specimens from southern HB and RS.

4.1 Hg in the abiotic compartment The concentrations of THg in groundwater (up to 251 µg L-1) and sediments (up to 2200 ng g-1) found in the vicinity of ECI, exceeded every existing ecological and health guidelines for Hg, in any kind of water and sediment (https://repository.library.noaa.gov/view/noaa/9327). For example, the ecological threshold value for groundwater is 2 µg L-1 in the USA. In Israel, the guideline for THg concentration in drinking water and the maximal guideline for seawater are 1 µg L-1 and 0.4 µg L-1, respectively. The groundwater pollution was apparent in the beach fresh water table up to a distance of nearly 3 km northward of the ECI, with concentrations ranging from 30 to 300 Page 15 of 34

Journal Pre-proof ng L-1 (Table S3, Fig. 2). For comparison, THg concentrations measured in groundwater reaching the sea were 52 ng L-1 in Massachusetts (Bone et al., 2007), 4 ng L-1 in Hawaiʻi (Ganguli et al., 2014), and 0.9 ng L-1, in filtered groundwater in the Yellow Sea (Rahman et al., 2013). In this study, THg concentrations in groundwater at the RS were <3 ng L-1, clearly demonstrating the polluted conditions in northern HB. Moreover, the apparent decreasing cross-shore gradient of THg in groundwater with increasing salinity demonstrates the mixing of ECI Hg enriched groundwater with seawater and the transport of

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THg to nearby coastal water.

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MeHg concentrations measured in the groundwater were low and constituted less than

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0.13% of THg (Table S3) except at the southern border of the ECI (station FM31) and 200

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m south of it (station FM39), with maximal relative contribution of 1.2% (Table S3). MeHg concentration decreased towards the sea, but its relative contribution to the THg increased to

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0.2-0.26% in the surf zone. This may suggest methylation of THg delivered to the sea during

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the groundwater transport, though by what mechanism is yet unknown. The optimal conditions for Hg methylation are anoxic, sulfate-containing sediments,

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enriched with biodegradable organic carbon and nutrients (Horvat, 1997). This can be seen in this study as well, by the correlations found between THg and MeHg, and between MeHg and TOC in the sediments of HB, as shown elsewhere (Conaway et al., 2003; Ravichandran, 2004; Sunderland et al., 2004). However, in this study, MeHg was detected in the sediment only when TOC concentrations were >1 wt.%, (Table S2a), and its relative contribution was positively correlated to THg (not statistically significant, but with a clear trend). Similarly, a previous study of sediments from the Qishon River estuary (Southern HB) showed that the relative contribution of MeHg and TOC concentrations were positively correlated when TOC was higher than 2%, and negatively correlated when TOC was less than 0.2% (Shoham-Frider et al., 2012). The semi-enclosed sites in HB (Akko marina and Haifa Port)

Page 16 of 34

Journal Pre-proof have characteristically high TOC and relatively high MeHg relative contribution as a result (0.5-0.9%, Table S2). Judging by the low TOC concentrations in ECI sediments, that were similar to the RS values, it is unlikely that the groundwater table is anoxic, yet the source of Hg – metallic and inorganic species and the presence of MeHg in the groundwater, clearly indicate that methylation is occurring. The presence of dissolved Hg in the groundwater (Table S3) might also enhance methylation, since its availability in sediment pore waters is a crucial step for the production of MeHg in the aquatic system (Oliveri et al., 2016). Hg from

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chlor-alkali plants reaching aquatic bodies by groundwater or surface water have been

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previously reported (Al-Majed BuTayban and Preston, 2004; Bravo et al., 2014; Oliveri et

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al., 2016; Sprovieri et al., 2011; Turner et al., 2018). Recently, it was shown that Hg

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discharged 50 years ago into Penobscot Estuary (Orrington, Maine, USA) from a chlor-

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4.2 Hg in Biota

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alkali plant, continues to be methylated in the estuary even today (Rudd et al., 2018).

Marine organisms exhibit a wide range of THg and MeHg concentrations, depending on

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taxonomic group and pollution in their habitat. In general, the concentrations at the base of the marine trophic web (phytoplankton and macroalgae) are lower than in the grazer mollusks and filter feeding bivalves and sponges, as found in this study. Recently, Cinnirella et al. (2019) published a compilation of mercury concentrations in biota from the Mediterranean Sea collected in surveys conducted over the last 40 years. The concentrations found in this study were similar or lower than those found at other coastal areas in the Mediterranean Sea (Fig. 5). Moreover, at the polluted sites of northern HB, THg concentrations have substantially decreased since 1980 by a factor of 2.5 in macroalgae, and 5.3 in grazing gastropods. Simultaneous records of THg and MeHg concentrations in biota

Page 17 of 34

Journal Pre-proof are less common in the literature, but when available, they show a similar dependency on pollution and trophic level as THg (Fig. 5). It is known that phytoplankton accumulates THg and MeHg mainly by passive uptake from the seawater that was shown to be the most important bioaccumulation step in marine food webs (Hammerschmidt et al., 2013; Lee and Fisher, 2016; Mason et al., 1996). The assimilation efficiency and bioaccumulation rates of MeHg are four times higher than inorganic-Hg, thus, its fraction from THg increases up the food web (Gosnell and Mason,

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2015; Mason et al., 1996; Mason et al., 2012). Recent laboratory experiments on MeHg

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uptake by 6 different algal class found volume concentration factors ranging from 0.2 to 6.4

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by passive uptake, with no correlation to temperature, light or nutrients (Lee and Fisher,

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2016). Uptake increased with temperature only in the dinoflagellate Prorocentrum minimum, suggesting an active uptake (Lee and Fisher, 2016) as seen elsewhere (Gosnell

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and Mason, 2015). The assimilation efficiencies of Hg+2 and MeHg by the copepod Acartia

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tonsa, an intermediate trophic link between phytoplankton and fish, ranged from 25% to 31% and 58% to 79%, respectively, depending on the Hg species present in its algal diets

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(Lee and Fisher, 2017). Suspension and filter feeder organisms are known to accumulate high concentrations of THg, mainly due to their efficient active filtration mechanisms (Langston, 1990), high particle retention rates (Stuart and Klumpp, 1984), and longevity (Batista et al., 2014), while Hg assimilation from the sediment can happen directly from it and/or by sediment re-suspensions (e.g. Dominik et al., 2014; Riisgård and Hansen, 1990; Shefer et al., 2015). Hg and MeHg assimilation efficiencies for grazers from their diet is <30% and 60-80%, respectively (Masson et al., 2012).

In this study, the spatial distribution of THg and MeHg concentrations in biota clearly demonstrate that the major source of Hg to HB is located in its northern region, most likely

Page 18 of 34

Journal Pre-proof the ECI plant. THg and MeHg concentrations were consistently higher in all taxonomic groups from the northern sites (SZ, Akko), compared to RS and southern HB (Table S4, Fig. 3). The relatively high concentrations found in biota from SZ, 7 km north of HB, were unexpected, considering its distance from the Hg source. However, the correlations found between PTHg and THg in seawater and sediments, indicate the presence of Hg-enriched suspended particles in seawater above Hg-contaminated sediments in HB (see section 3.1). These particles are also transported northwards by the prevailing alongshore northerly

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current (Rosentraub and Brenner, 2007) out of HB during and following resuspension events

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associated with winter storms, as shown by Bareket et al. (2016).

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Unfortunately, in this study, due to the lack of sample material, MeHg was not analyzed in

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plankton and its fraction from THg is unknown and remains to be investigated. However, the relative contributions of MeHg in specimens of the bivalve S. spinosus and the sponge I.

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variabilis from Akko and SZ were higher with a constant offset than the enrichment found

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in specimens from RS and southern HB, at the same THg concentrations (Fig. 4, Table S4). This indicates that the presence of MeHg in northern HB is more significant than in RS and

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southern HB. The high MeHg relative contribution in the macroalga G. rugosa from Akko but not from RS (34% vs. <0.01%) also indicates the presence of MeHg in seawater and its assimilation directly from it. Similarly, MeHg enrichment was greater in the limpet Patella sp. from ACH, Akko and QY compared to RS specimens. The lowest enrichment in Patella sp. was found in specimens collected from Haifa Port, where the MeHg concentrations in the sediments were the highest found in this study (Table S2). However, limpets do not live in the sediment, but on hard substrates. Moreover, they have been shown to feed on an assortment of benthic macroalgae and microalgae, algal propagules, biofilm as well as small invertebrates (e.g. Notman et al., 2016). Therefore, it is possible that MeHg in Patella sp. from Haifa Port did not originate from the sediments. Moreover, it implies that the food

Page 19 of 34

Journal Pre-proof sources in the port are less polluted by MeHg than at the other stations, excluding RS. However, it should be noted that THg concentrations in Patella sp. from Haifa Port did increase perceptibly and declined afterwards over the period 2005-2009 during which port development operations very likely caused resuspension of polluted sediments and increased accumulation (Shefer et al., 2015).

4.3 Seasonality

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Based on hydraulic differences and Darcy’s equation, it was previously estimated that the

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groundwater below the ECI plant flows into the sea with a velocity of ca. 50 meters per year

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(Greytzer, 2000). However, the use of groundwater by the ECI stopped when the plant

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closed down in 2003 and the aquifer near the plant has been recharged every winter since. This could have caused an increasing trend in groundwater discharge into the sea and hence

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increased the load of Hg to the marine environment observed in northern HB since 2006.

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Furthermore, seasonality demonstrated by higher concentrations of THg in shore seawater and in sands of the municipal bathing beaches of Akko, in spring compared to summer,

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strongly support the hypothesis that ECI groundwater flow to the sea is regulated by the precipitation regime. An additional factor for the observed seasonality could be the influence of marine microbes to the evasion of Hg and MeHg from surface seawater into the air, which increases with temperature (Lee and Fisher, 2019). However, despite the apparent seasonality of THg in shore waters and beach sediments, the THg in plankton did not exhibit a corresponding seasonality, possibly due to the small sample size (Table 5).

Conclusions All the recent findings presented and discussed here support our hypothesis that at present, the source of Hg and MeHg enrichment in biota from northern HB is the discharge of

Page 20 of 34

Journal Pre-proof polluted groundwater along the ECI shoreline, a legacy from the ECI plant that was operated with little concern for the environment. The increased Hg burden found in fish from northern HB during 2006-2014, following more than a decade of decreasing concentration, is likely the result of the recharge and increased hydraulic head of the shallow water coastal aquifer in the area following the shutdown of the ECI and cessation of groundwater pumping for the industrial process in 2003. These findings demonstrate the potential of relic pollution in groundwater to increase heavy metal burdens in local marine food webs.

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However, the dynamics and timing of the changing trends as well as the Hg methylation

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processes remain unclear.

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Acknowledgments

This research was funded by the Israel Ministry of Environmental Protection, grant no. 145-

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1-1. We thank Ms. Hana Bernhard for drawing the figures. We are greatfull to three

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anonymous reviewers for their thorough remarks that helped improved this manuscript.

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Processes in the Marine Environment. UNEP, Athens, Greece, pp. 369–381.

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Journal Pre-proof Figure 1. Map of Haifa Bay and sampling sites in the Bay and coastal areas to the north and south of it. Inset, map of sampling stations in the northern part of Haifa Bay and the chlor-alkali plant (ECI) area. Sampling stations are indicated by filled black circles, lines indicate tow lines of plankton nets and stars indicate sampling by SCUBA divers. Figure 2. THg concentrations in sediments and groundwater along the seashore northwards (positive values in the x-axis) and south-wards (negative values) from the chlor-alkali plant (ECI, FM 32 =zero). Grey triangles, black circles and white squares represent samples at the shoreline, 30 m, and 125 m inland, respectively. Note: The Y axis in panel C is presented in logarithmic scale

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Figure 3. Box-whiskers plots of THg in plankton and THg and MeHg concentrations in the bivalve S. spinosus from the different sampling sites. Upper and lower limits (whiskers), bottom and top of box 1st and 3rd quartiles, band inside the box is the median and the cross is the average. Outliers are located outside the whiskers. Significant differences are marked.

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Figure 4. Relative MeHg contribution to THg (MeHg/THg ) as a function of THg concentrations in the bivalve S. spinosus and the sponge I.. variabilis from different sampling sites.

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Figure 5. THg and MeHg concentrations (ng·g-1) in marine biota from polluted and non-polluted sites in the Mediterranean Sea. Error bars denote ±95% confidence intervals.

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Journal Pre-proof

Legacy groundwater pollution as a source of mercury enrichment in marine food web, Haifa Bay, Israel

Shoham-Frider E.1*, Gertner Y.1, Guy-Haim T.1, Herut B.1, Kress N.1, Shefer E.1 and Silverman J.1

Israel Oceanographic and Limnological Research, Haifa 31080, Israel

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* Corresponding Author: [email protected]

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Conflict of Interest Statement

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The authors have no conflict of interest regarding this manuscript.

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Journal Pre-proof Table 1: Details of the sampling sites and stations occupied during this study. a) Dates, sites and environmental matrices sampled during the study (HB-Haifa Bay, ECI-chloralkali plant, RS-Reference site, QY- Qiryat Yam, SZ-Shavey Ziyon, ACH- Achziv) Site Environmental matrix sampled HB and RS Seawater, SPM, marine sediment, plankton ECI Groundwater March 2015 HB and RS Mollusca, macroalgae, sponges May 2015 ECI Groundwater and inshore sediment HB and RS Plankton July 2015 Akko municipal beaches Groundwater and seawater August 2015 Akko municipal beaches Inshore and marine sediment December 2015 Haifa Port and QY Mollusca April 2016 HB , SZ and RS Plankton Akko municipal beaches Seawater and inshore sediment ECI Groundwater and seawater May 2016 ACH, Akko, QY and Mollusca and macroalgae RS July 2016 SZ, Akko and RS Plankton SZ, Akko, HB and RS Mollusca, macroalgae, sponge * Seawater and SPM sampled at the surface and near the bottom (Table S2).

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Date February 2015*

b) Sampling stations at each site. See also Figure 1 and Table S1.

RS ECI

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Stations FM1- inside marina Akko, FM2- nearshore station off marina Akko, FM5 - nearshore station off ECI, FM6- Entrance to Haifa Port, FM7- Western Haifa Port, FM8- Entrance to Qishon Fishing Port. FM10 area FM3, FM4, FM30 - FM35. Station FM31 and FM33 were located at the southern and northern perimeters of the ECI, respectively. Stations FM3, FM4 and FM31 were located within the ECI. Station FM30 was located ca. 220 m south of station FM31 and stations FM34 and FM35, 325 and 620 m north of station FM33, respectively.

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Stations with the suffix a, b, c, indicate: a, at the shoreline, b and c up to 30 m from the shoreline Akko municipal bathing beaches 

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FM36 - FM43. Station FM36. The southernmost of the Akko municipal beaches was located ca. 1km from station FM33

Journal Pre-proof Highlights Hg discharged into the marine environment polluted the Northern Haifa Bay (Israel)

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Gradual reduction of Hg discharge decreased concentrations in biota and sediments

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Unexpected increase in Hg concentration in fish observed from 2006 to 2014

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Hg levels were higher in the environment and biota near a chlor-alkali plant (ECI)

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Relic Hg seeping into the groundwater from the ECI is the source of Hg to the sea

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Figure 1

Figure 2

Figure 3

Figure 4

Figure 5