Mercury forms in the benthic food web of a temperate coastal lagoon (southern Baltic Sea)

Marine Pollution Bulletin 153 (2020) 110968

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Mercury forms in the benthic food web of a temperate coastal lagoon (southern Baltic Sea)

T

Agnieszka Jędruch , Magdalena Bełdowska ⁎

Institute of Oceanography, University of Gdańsk, Piłsudskiego 46, 81-378 Gdynia, Poland

ARTICLE INFO

ABSTRACT

Keywords: Labile mercury Biomagnification Benthic macrofauna Coastal zone Baltic Sea

The study was conducted in the coastal zone of the southern Baltic. The research material consisted of macrozoobenthos and elements of its diet. The samples were analysed for Hg and its labile and stable forms, using the thermodesorption method. The results showed that the level of total Hg in zoobenthos was associated with dietary preferences and the share of bioavailable Hg in its food. The Hg fractionation in the macrofauna was conditioned by biological features (morphological structure) and environmental parameters (oxygenation, pH) which shape the mobility and assimilation of Hg. The absorption of the most toxic organic Hg in macrofauna was more effective in aerobic conditions, at low primary production and with the limited inflow of organic matter. The trophic transfer of Hg was favoured by the limited biomass of primary producers, and consequently of zoobenthos. An important factor influencing the biomagnification was also the share of labile Hg in macrozoobenthos.

1. Introduction Mercury (Hg) has been the subject of numerous scientific studies over many years. This is mainly related to the chemical and biological activity of Hg, its high mobility, rapid spread in the environment and the ability to bioaccumulate and biomagnify (Fröstner and Wittman, 1981; Jackson, 1998). As a chemical substance, Hg can exist in several forms, such as inorganic Hg, which includes metallic Hg and Hg vapour (Hg0) and mercurous (Hg22+) or mercuric (Hg2+) salts; and organic Hg, which includes compounds in which Hg is bonded to a structure containing carbon atoms (methyl, ethyl, phenyl, or similar groups). The form of Hg determines its toxicity – the most toxic are the organic Hg compounds, such as methylmercury (MeHg) (Berlin et al., 2007). Numerous research confirm the negative impact of Hg not only on humans (WHO, 2003; Bose-O'Reilly et al., 2010; Jan et al., 2015) but also animals, including invertebrates. These studies show that Hg can led to several physiological, morphological and behavioural disorders and consequently adversely affected the metabolism, reproduction and development of organisms (Hammerschmidt et al., 2002; Scott and Sloman, 2004; Gorski and Nugegoda, 2006; Weis, 2014; Morcillo et al., 2017; Barboza et al., 2018; Cappello et al., 2018). The most important sources of Hg in the marine environment are rivers transporting contaminants leached from the catchment area, as well as wet and dry atmospheric deposition (HELCOM, 2010;

⁎

Bełdowska et al., 2016a). A significant amount of Hg undergoes accumulation close to the coast, especially in bottom sediments, from where it can be incorporated into the trophic chain by benthic flora and fauna (Bełdowska et al., 2015, 2016b; Jędruch et al., 2018a). The major routes of Hg entry into the marine organisms are uptake of forms dissolved in the water column and sediment porewater, uptake of fine particulate forms, and transfer from food (Lawrence and Mason, 2001; Soto et al., 2011; Bełdowska et al., 2018a). In the case of primary producers, the Hg uptake from the surrounding water is the dominant process, whereas for animals the importance of the food intake becomes more important as their position in the food chain increases (Soto et al., 2011). Benthic invertebrates are an important element of the marine ecosystem – they are in the intermediate position in the trophic chain, functioning as a ‘trap’ for all sources of food (i.e. phytoplankton, macrophytes, land-derived detritus) and constitute a significant ingredient in the diet of many fish, birds and marine mammals, as well as humans (Armstrong, 1987). Moreover, the consumption of fish and seafood is the main source of Hg in the human body (Boening, 2000). The level of Hg concentration in benthic organisms depends on the size of Hg load into the marine environment, the primary production conditioning the biomass of organisms, and also on the hydrodynamic conditions of the environment affecting its physical and chemical parameters (Pempkowiak, 1997; Chen et al., 2008; Chouvelon et al., 2018; Jędruch et al., 2018a). Parameters such as pH, temperature or

Corresponding author. E-mail address: [email protected] (A. Jędruch).

https://doi.org/10.1016/j.marpolbul.2020.110968 Received 27 August 2019; Received in revised form 4 February 2020; Accepted 6 February 2020 Available online 13 February 2020 0025-326X/ © 2020 Elsevier Ltd. All rights reserved.

Marine Pollution Bulletin 153 (2020) 110968

A. Jędruch and M. Bełdowska

Fig. 1. Location of research stations in the coastal zone of Puck Lagoon (southern Baltic Sea, Poland).

oxygenation of water and sediments affect the accumulation of Hg in benthic organisms. This is because, on the one hand, they regulate the metabolism and functioning of the benthos (including filtration rates and bioturbation) (Bonaglia et al., 2013; Weis, 2014), and on the other hand, they determine the changes and mobility of Hg at the water-sediment interface (Jędruch et al., 2018a, 2019b). They also affect the bioavailability of Hg, conditioning the chemical form of Hg in the benthic zone (Bełdowski et al., 2018). Studies on Hg concentration in benthic organisms have been conducted for many years, however, most of these were concerned only with the total Hg level (HgTOT) (i.e. Falandysz, 1994; Odžak et al., 2000; Boszke et al., 2003b; Airas et al., 2004; Kayhan, 2007; Taylor et al., 2012; Meng et al., 2015; Jędruch et al., 2018a, 2019b) or MeHg (i.e. Andersen and Depledge, 1997; Classie et al., 2001; Loukmas et al., 2006; Molina et al., 2010; Chen et al., 2014; Gosnell, 2016). However, the HgTOT concentrations give incomplete information in terms of the potential hazard of Hg. It is similar in the case of MeHg, which although is the most toxic form of Hg, it is not the only one which can be included in the trophic chain and pose a threat to organisms (Broussard et al., 2002; Bradley et al., 2017). The form in which Hg occurs in the environment is particularly important because only loosely bound or dissolved Hg compounds can be absorbed in the tissues of organisms, and reach elevated concentrations in higher-order consumers as a result of biomagnification (Jackson, 1998). In terms of Hg binding to the solid matrix, it is possible to differentiate between two groups of accessibility for the environment - the first are weakly bound, bioavailable labile forms, the second are stable forms, strongly bound to the matrix (Bełdowski and Pempkowiak, 2003; Boszke et al., 2003a). Labile Hg forms include Hg halides, Hg

bound with humic substances or ligands (which have strong complexing properties), as well as the most toxic organic forms (Sadiq, 1992; Broussard et al., 2002). Stable Hg forms include HgS and residual Hg, often bound with the mineral matrix. Another stable and highly insoluble Hg compound is HgSe, which is formed under reducing conditions occurring in the bottom sediments, similar to HgS (Flores-Arce, 2007). The latter forms are characterized by the lowest toxicity and low bioavailability for organisms. Under certain conditions, stable forms can also be transformed into labile forms, e.g. HgS can be transformed into an organic form with the participation of sulphate-reducing bacteria and fungi (Martin-Doimeadios et al., 2004). The number of studies on labile and stable forms of Hg in organisms from the base of the aquatic food chain is low, which is mainly caused by limitations of sample collection and individual size of organisms (Taylor et al., 2008). Current approaches to Hg speciation require separate chemical extraction and/or digestion of sample, therefore, relatively much research material is required. The analysis of low-mass samples, such as benthic invertebrates is possible with the newly-developed thermodesorption method (Jędruch et al., 2018b). The use of this method enabled the recognition of the participation of individual Hg forms in these ecologically important benthic organisms. As shown in the previous preliminary studies of the authors conducted in the southern Baltic Sea (Gulf of Gdańsk and the Vistula Lagoon), in the case of macrozoobenthos, the total share of labile forms in HgTOT was higher than 90% (Jędruch et al., 2018a, 2019a; Wilman et al., 2019). This value significantly exceeds the proportion of MeHg in HgTOT in the tissues of benthic invertebrates, which ranged from 30 to 70% (Andersen and Depledge, 1997; Margetínová et al., 2008; Jędruch et al., 2

Marine Pollution Bulletin 153 (2020) 110968

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2018a). That indicates that an important share of other, rarely studied, bioavailable forms of Hg (such as Hg halides, Hg complexes with organic matter, and Hg sulphate), can account for as much as 60% of HgTOT. Importantly, the results obtained by the authors showed that almost the entire Hg load accumulated in zoobenthic organisms can be transferred to higher trophic levels - to fish, marine mammals, as well as to humans. However, it is important to recognise the factors that determine the level of labile Hg in the bottom fauna organisms, which, due to their sedentary lifestyle, can act as biological indicators of marine environment pollution (Luoma and Rainbow, 2008; Soto et al., 2011). This study aimed to determine the share of individual Hg forms (labile and stable), using the thermodesorption method, in the macrozoobenthic organisms of the marine coastal zone, collected at research stations with diverse sources of organic matter (terrigenous or marine material) and different environmental parameters.

making sure that each sample contained an entire plant. Surface sediments (ca. top 10 cm layer) were collected using a Van Venn sampler and placed in zip lock bags. On each occasion, the ancillary parameters of the water (temperature, salinity, pH) and surface sediments (oxidation-reduction potential) were measured, using a ProfiLine Multi 3320 field meter (WTW, Poland). The portable meter was calibrated before each sampling campaign (the procedure included the use of buffer solution and 0.1 M KCl). After transportation to the laboratory, the taxonomic composition of macrozoobenthos was analysed. The organisms were counted and determined to species level or a higher systematic unit, using a stereoscopic microscope. Taxonomic identification of organisms was carried out based on observations of their morphological characteristics and using taxonomic keys (Żmudziński, 1990; Barnes, 1994). The preparation of samples for Hg analysis involved the placement of taxonomically sorted biological material into weighed Eppendorf tubes, previously cleaned by soaking for 24 h in 4 M HNO3. The near-bottom water samples were filtered through previously combusted (500 °C, 6 h) preweighed Whatmann GF/F glass microfiber filters (pore size: 0.7 μm, diameter 47 mm) in order to separate the suspended particulate matter (SPM). The collected macrophytes were cleared of epiphytes, organic and mineral particles, and then rinsed with Milli-Q water. A taxonomic analysis of the plant material was also conducted using the taxonomy key given by Braune and Guiry (2011). Sub-samples were separated from the collected surface sediments, in which ancillary physical parameters were analysed: organic matter content expressed as loss on ignition (LOI) (550 °C, 6 h) (Santisteban et al., 2004) and granulometric distribution determined by sieving through a set of normalised diameter mesh sizes, according to the Wentworth (1922) sediment grainsize classification. The collected biological material, filters with suspended matter and the sediments were then stored at −20 °C. Before proceeding with chemical analyses, samples were freeze-dried (Alpha 1–4 LDplus, Martin Christ, Germany). Then the samples (except for filters) have been homogenised in a ball mill (8000 M Mixer/Mill, SPEX SamplePrep, USA) with an agate vessel.

2. Materials and methods 2.1. Study area The research was conducted at two research stations in the coastal zone of the Puck Lagoon, located in the southern part of the Baltic Sea (Fig. 1). As with the whole of the Baltic Sea, the Puck Lagoon has for many years been exposed to an uncontrolled inflow of Hg-containing pollutants from surrounding areas that are either heavily urbanised or agricultural - pastures and arable fields. This resulted in increased concentration of Hg in bottom sediments (Bełdowski and Pempkowiak, 2003; Jędruch et al., 2015; Kwasigroch et al., 2018) and benthic organisms in comparison with open regions of the Polish coast (Bełdowska et al., 2015, 2016b; Jędruch et al., 2019a, 2019b). The Puck Lagoon, and its inner part in particular, is also an exceptionally valuable natural area being characterized by great biodiversity and high biomass of organisms. The most important distinguishing feature of the Puck Lagoon is its underwater meadows of seagrass, which are very important habitats for numerous invertebrate species, also offering shelter for fish spawn and fry (Węsławski et al., 2013; Jankowska et al., 2018). The research station located on the western shore of the Puck Lagoon (Osłonino) is characterized by a large load of land-derived organic matter associated with the inflow of rivers and the erosion of the cliff coast in the area of the station (Fig. 1). The terrigenous organic matter also accumulated in the coastal zone in the area of this station owing to the shape of the shoreline and low water dynamics. On the other hand, the sampling station located in the northern part of the Puck Lagoon (Chałupy) is under the limited influence of the land - the Hel Peninsula, located in the immediate vicinity of the station, is only 240 m wide, and the shoreline is protected against abrasion by a concrete seawall. As a consequence, the main sources of the organic matter here are primary production in situ and marine material transported from the open parts of the sea (Bełdowska et al., 2016a; Jędruch et al., 2017).

2.3. Chemical analyses The analysis of individual mercury forms was carried out on a DMA80 analyser (Milestone, Italy), according to the method of Hg compound thermodesorption (Saniewska and Bełdowska, 2017). This method is based on the comparison with the sequential volatilization of a series of known Hg compounds heated incrementally between 50 °C to 750 °C (Saniewska and Bełdowska, 2017; Bełdowska et al., 2018a). The heating temperature, time to reach the target temperature and time at the target temperature for which the highest Hg level was measured were directly controlled according to the guidelines presented by Saniewska and Bełdowska (2017). The 5-step thermodesorption method allows for the isolation of five groups of Hg compounds with similar properties (Bełdowska et al., 2018a; Jędruch et al., 2018b). The first fraction, released at the lowest temperature of 175 °C (heating time: 9 min), consists of the most labile Hg compounds (HgCl2, HgBr2, HgI2, Hg(CN)2) (Hg labile 1a). The forms released at the next temperature step of 225 °C (heating time: 8 min) are labile Hg compounds bound with humic substances, MeHg, as well as other Hg compounds formed with strongly complexing ligands ((CH3COO)2Hg, Hg(NO3)2∙H2O, Hg(SCN)2, Hg (ClO4)2∙xH2O) (Hg labile 1b). At 325 °C (heating time: 12 min) the insoluble, stable Hg sulphide (HgS) underwent decomposition. At 475 °C (heating time: 10 min), the forms that decomposed were mainly semilabile compounds: HgO, HgSO4 and HgF2 (Hg labile 2). At the highest temperature of 750 °C (heating time: 6 min), the decomposed Hg compounds were bound with the residual fraction, a form which was not available to the environment (Hg residual) (Jędruch et al., 2018a). Samples were weighed on quartz boats and the sample mass was 0.05–0.1 g. The analysis of Hg forms in the collected environmental

2.2. Sample collection and preparation for analysis Samples from ca. 1 m depth were collected during August and September 2017 field campaigns. Macrozoobenthos were collected using a Van Veen sampler (HYDRO-BIOS, Germany) with a surface area of 250 cm2, in three replicates. In order to separate organisms from the sediment, the collected organisms were wet-sifted and retained by a 0.5 mm sieve. The living biological material was placed in aerated containers filled with seawater and then transported to the laboratory in accordance with the method previously described by Bełdowska et al. (2016b). Near-bottom water was collected directly into 1 L borosilicate glass bottles in three replicates. Bottles were previously cleaned with 4 M HNO3, rinsed with Milli-Q water and combusted (300 °C, 6 h). Macrophytobenthos was collected by hand into polythene zip lock bags, 3

Marine Pollution Bulletin 153 (2020) 110968

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samples was carried out in at least three replicates (in the case of zoobenthos, that number was higher if the mass of the collected organisms was sufficient). The accuracy of the analysis was verified by comparing the sum of Hg concentrations measured by the 5-stage fractionation method with the result of the Hg total analysis (HgTOT) carried out by incinerating the sample at 750 °C (Saniewska and Bełdowska, 2017). The accuracy of the Hg form analysis was 94% on average, with a standard deviation not exceeding 5%. The quality of the method was also checked by an analysis of certified reference materials (tea leaves INCT-TL-1 – HgTOT: 5 ng g−1, soil NCS DC 87103 – HgTOT: 17 ng g−1, plankton BCR-414 – HgTOT: 276 ng g−1), carried out in triplicate (sample weight: 0.1–0.2 g), for which the average recovery ranged from 96 to 105%. Limit of detection (LOD) was calculated according to IUPAC (1997) equation:

LOD = x blank + k SDblank

The slope of this regression (B) is the TMS (Broman et al., 1992), a parameter which is routinely used as an indicator of the biomagnification potential of Hg. Assuming that a change of stable nitrogen isotope of 3.4‰ represents one trophic level (Hobson and Welch, 1992), the biomagnification factor (BMF), representing the increase of Hg concentration per trophic level, was calculated on the basis of antilogarithmic back-transformation:

BMF = e3.4B 3. Results and discussion 3.1. Environmental conditions of the near-bottom zone

The two research stations in the Puck Lagoon, despite being located at a relatively short distance from each other (about 10 km) (Fig. 1), differed in terms of the environmental parameters of the benthic zone: sediments and near-bottom water (Table SI). Despite the fact that the fraction of medium sands dominated in the surface sediments at both stations (grain diameter 250–500 μm), in the case of Chałupy, the share of fine sediment fraction (FSF) (grain diameter < 63 μm) was more than two times lower (mean: 0.6%) than in the case of Osłonino (mean: 1.4%). The sediments in Chałupy were also poorer in organic matter, as evidenced by the LOI value which was three times lower (mean: 0.4%) compared to the station in Osłonino (mean: 1.2%) (Table SI). The characteristics of surface sediments in the area of these stations were shaped mainly by the dynamics of the environment - the station in Osłonino is located in a shallow bay where the exchange of water is limited, allowing for the deposition of fine sediments. In the area of Osłonino, an increased inflow of suspended particulate matter (SPM), introduced into the basin together with rivers that discharge in this area and as a result of coastal erosion was also observed. This is evidenced by the concentration of SPM in water, which was over three times higher at the station in Osłonino (mean: 23.4 mg dm−3) than at the station in Chałupy (mean: 7.1 mg dm−3) (Table SI). The increased concentration of organic matter in sediments in the area of Osłonino is, in turn, associated with higher primary productivity in the area of this station. During the research period, the primary production in Osłonino (mean: 19.6 mg m−2 d−1) was twice as high as in the case of Chałupy (mean: 9.1 mg m−2 d−1), while the concentration of cyanobacteria in Osłonino (mean: 250 mg m−3) was over 60% higher than in Chałupy (mean: 150 mg m−3) (model.ocean.univ.gda.pl). The intensive inflow of organic matter, both autochthonous and allochthonous, to sediments in the area of Osłonino, resulted in hypoxic conditions. Although the Eh potential values indicate prevailing reductive conditions at both stations, in Osłonino Eh was several-fold lower (mean: −211.7 mV) than in Chałupy (mean: 34.7 mV) (Table SI). A similar situation was observed in the case of dissolved oxygen concentration in water, which at the Osłonino station (mean: 4.4 mg dm−3) was about 60% higher than in Chałupy (mean: 7.1 mg dm−3). The near-bottom water in Osłonino was also characterized by a lower pH (mean: 7.4) compared to the station in Chałupy (mean: 7.7). This is important, given the fact that oxygen conditions and pH are important parameters determining the mobility and bioavailability of Hg in the marine environment, as well as the physiology of bioaccumulation of the metal in organisms that live in bottom sediments or feed on them (Pempkowiak, 1997; Kidd et al., 2012; Jędruch et al., 2018a).

(1)

where x̄blank is the arithmetic mean of 10 blank (analyte-free samples) measurements, SDblank is the blank standard deviation, and k is a numerical factor. The value chosen for k was 3 as recommended by IUPAC (1997). The LOD was calculated for each of the five fractionation temperatures. In any case, the calculated LOD did not exceed 0.01 ng of Hg. 2.4. Processing results Statistical analysis of the obtained results was carried out using STATISTICA 12 software (StatSoft). The analysed data were characterized by the normal distribution (Shapiro-Wilk test, p > 0.05). To determine the significance of the difference between data sets from two sampling stations, the t-test was used (p < 0.05). The relationships between the analysed variables were determined on the basis of the Pearson correlation coefficient, with a confidence interval of at least 95%. The map of the study area with the distribution of sampling stations was created using ArcMap 10.4 software (ESRI) with the geographic coordinate system chosen for data presentation WGS 1984. The spatial data were provided courtesy of the GIS Centre, University of Gdańsk (www.ocean.ug.edu.pl/~oceju/CentrumGIS). 2.4.1. Determination of Hg bioaccumulation and biomagnification To evaluate the ability of benthic organisms to accumulate Hg from surface sediment, the biota-sediment accumulation factor (BSAF) was calculated following the formula suggested by Szefer et al. (1999):

BSAF =

Hgbiota (2)

Hgsediment

where Hgbiota and Hgsediment are the concentrations of Hg in a given taxon and surface sediments, respectively. In order to determine Hg accumulation in the trophic chain the theoretical model, developed by Broman et al. (1992) and Rolff et al. (1993) for the trophic transfer of contaminants was applied:

Hgcompartment = AeB

15

N

(3)

where Hgcompartment is the HgTOT concentration in sediments, particulate suspended matter and benthic organisms, and A and B are the function parameters of Hg concentration and nitrogen isotopic value (δ15N). The data on the stable isotope ratio of nitrogen (δ15N) values in selected ecosystem components used in this study can be found in supplementary material (Table SV), as well as in the previous works of the authors (Jędruch et al., 2018b; Jędruch et al., 2019b). The model constant A is a scaling factor that depends on Hg concentration at the base of the food chain (Rolff et al., 1993). In order to estimate the parameters A and B, variables from Eq. 2 were converted using logarithmic transformation, resulting in linear regression:

ln Hg compartment = B

15N

+ lnA

(5)

3.2. Macrozoobenthos structure In the samples of macrozoobenthos collected in the coastal zone of the Puck Lagoon, a total of 14 taxa typical of the study area (Janas and Kendzierska, 2014) were observed (Fig. SI, Table SII). The zoobenthos consisted of bivalves: lagoon cockle (Cerastoderma glaucum), Baltic clam (Limecola balthica), and blue mussel (Mytilus trossulus); crustaceans: amphipods (Corophium sp. and Gammarus sp.), an isopod (Idotea sp.),

(4) 4

Marine Pollution Bulletin 153 (2020) 110968

A. Jędruch and M. Bełdowska

Fig. 2. Species composition, a) abundance, and b) biomass of benthic macrofauna at research stations in the coastal zone of Puck Lagoon (for details, see Table SII).

of macrozoobenthos on the seabed. The abundance of organisms at the station in Chałupy was almost two times lower (mean: 12940 ind m−2), compared to the station in Osłonino (mean: 21013 ind m−2) (Fig. 2a). A similar tendency was observed for macrofauna biomass - in Chałupy it was over 2 times lower (mean: 54 g m−2) compared to Osłonino (mean: 139 g m−2) (Fig. 2b). The species diversity of zoobenthos, as well as its abundance and biomass, in Chałupy and Osłonino, is associated with the different environmental conditions at the stations, the type of bottom sediments, and above all with the type of habitat and availability of food (Kotwicki, 1997). The Chałupy area is characterized by the occurrence of underwater meadows of seagrass Zostera marina and mixed brackish vascular plants (Potamogeton sp., Ruppia sp., Zannichellia sp.), which constitute very good habitats for macrozoobenthos (Węsławski et al., 2013; Jankowska et al., 2014). This resulted in a larger biomass of herbivore grazers feeding on benthic macrophytes, such as Peringia sp., Theodoxus fluviatilis or Idotea sp. (Muus, 1967; Morrisey, 1988) (Fig. 2b). These organisms also attained larger sizes - in Chałupy, the biomass of an individual organism of the Theodoxus fluviatilis was more than two times higher than in Osłonino station. In the case of Idotea sp. and Peringia sp., the difference in the individual biomass at research stations was 33% and 15%, respectively. Due to strong eutrophication, the ecological value of the Osłonino area is much lower compared to the station in Chałupy, despite the large biomass of macrozoobenthic organisms (Węsławski, 2009). In Osłonino, the macroalgae biomass was about two times lower, and the dominant taxon, apart from Potamogeton sp., was the filamentous brown algae Pilayella littoralis (Bełdowska et al., 2016b). The mass occurrence of filamentous algae provides evidence for intensive eutrophication. Moreover, this species reduce the growth of valuable seagrass and has a detrimental effect on the bottom fauna (Kruk-Dowgiałło, 1996). The intensive inflow of SPM, mainly of terrigenous origin (Jędruch et al., 2017), was conducive to the

and the dwarf crab (Rhithropanopeus harrisii); gastropods: laver spire shells (Peringia sp.) and freshwater snail (Theodoxus fluviatilis); polychaetes: ragworm (Hediste diversicolor) and the red-gilled mud worm (Marenzelleria sp.); oligochaetes; ribbon worms Nemerta; and insect larvae. The species composition of macrozoobenthos was similar at both of the sampling stations - 12 taxa were observed in the area of Chałupy, and 11 in Osłonino. However, the proportions in which the individual taxa occurred at these stations were different (Table SII). In Chałupy, the total number of organisms was dominated by snails, which accounted for half of the organisms (mean: 51%) (Fig. 2a). Among them the most numerous one was Peringia sp., constituting on average 36% of the macrozoobenthos at that station. An important component of the benthos in Chałupy was the crustacean Idotea sp., which on average constituted 24% of the total number of organisms. Peringia sp. was also predominant in the biomass of macrofauna in Chałupy (mean: 28%). The other snail Theodoxus fluviatilis (mean: 21%) and clam Cerastoderma glaucum (mean: 19%) also had significant shares in biomass (Fig. 2b). The average share of other taxa in the macrozoobenthos at Chałupy station biomass did not exceed 10% (Table SII). As in the case of Chałupy, Peringia sp. was the most numerous of the taxa identified in Osłonino although its share was much higher (mean: 44%) (Fig. 2a). The second most numerous species in Osłonino was the clam Limecola balthica (mean: 20%). On the other hand, the biomass of organisms in Osłonino was largely dominated by Cerastoderma glaucum, the share of which accounted for more than a half (mean: 56%) of the combined mass of all organisms (Fig. 2b). Limecola balthica also had an important share in the biomass (mean: 20%) and so did Peringia sp. (mean: 19%). The share of other taxa in the biomass was insignificant - in total, they constituted only an average of 3% of macrozoobenthos biomass in the area of Osłonino (Table SII). Apart from differences in the taxonomic composition, the research stations also differed in terms of the density 5

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the snail Theodoxus fluviatilis (mean: 36.6 ng g−1) (Jacoby, 1985). Importantly, herbivores accounted for more than half (mean: 57%) of the biomass of macrozoobenthos in Chałupy (Fig. 2; Table SII). In a different group of macrofauna: the suspension-feeding mussels, which constituted an important share of the total biomass (mean: 25%) (Fig. 2; Table SII), the HgTOT concentration was much lower than in the grazers. The lowest HgTOT concentrations among the taxa identified in Chałupy were measured in Limecola balthica (mean: 18.8 ng g−1), while in another suspensivore - Cerastoderma glaucum, the HgTOT concentration was not much higher (mean: 27.4 ng g−1) (Fig. 3). The lowest concentrations of HgTOT in the filter-feeders at the Chałupy station were associated with the fact that the HgTOT concentration in their food, SPM, was lower compared to Osłonino (mean: 41.9 ng g−1) (Table SIII). The SPM was also characterized by a lower share of the most bioavailable, adsorbed labile fraction of Hg (Hg labile 1a) (mean: 26.9%), which was 13 percentage points lower than in Osłonino (Fig. 4a). In the case of the remaining 5 taxa found at the station in Chałupy, the mean HgTOT concentrations ranged from 29.7 ng g−1 in Hediste diversicolor to 42.6 ng g−1 in Gammarus sp. (Fig. 3). These taxa are classified as omnivorous organisms, and their diet can be both organic matter deposited in sediments and animal tissues (Muus, 1967; Olivier et al., 1995; Olenin and Daunys, 2005). At the station of Osłonino the highest HgTOT concentrations were measured in polychaetes Marenzelleria sp. (mean: 50.6 ng g−1) and in Hediste diversicolor (mean: 48.5 ng g−1) (Fig. 3). These taxa are omnivorous, but they also enrich their diet with food of animal origin - they can be both predators and scavengers. However, the contribution of these organisms in the zoobenthos biomass in Osłonino was small (about 1%). The macrofauna biomass in this region was dominated by mussels Cerastoderma glaucum and Limecola balthica, which jointly accounted for as much as 75% of the total mass of organisms (Fig. 2). These species were characterized by a higher HgTOT concentration than average, especially in the case of Cerastoderma glaucum (mean: 42.6 ng g−1) (Fig. 3). High concentrations of Hg in these filter-feeders were associated with the HgTOT level in SPM (mean: 74.6 ng g−1) which was almost twice as high as in Chałupy (Fig. 3; Table SIII), as well as with the higher proportion of Hg loosely bound on suspended particles (Hg labile 1a) (mean: 39.5%) (Fig. 4b). Elevated HgTOT concentrations in the filter-feeders could also have been caused by the low mass of individual specimens - the average weight of a single Cerastoderma glaucum in Osłonino was almost two times lower than in Chałupy, while in the case of Limecola balthica it was four times lower. This combined with the consumption of Hg-rich SPM led to a high level of the Hg in their tissues. Elevated concentrations of HgTOT were also measured in another taxon that feeds on suspended matter - Corophium sp. (Olenin and Daunys, 2005) (mean: 46.2 ng g−1) (Fig. 3). In the case of herbivorous grazers, constituting a total of 20% of macrozoobenthos biomass in Osłonino (Fig. 2; Table SIII), HgTOT concentrations ranged from 23.6 ng g−1 in Peringia sp. to 27.6 ng g−1 in Theodoxus fluviatilis (Fig. 3) and were approximately twice as low as the values measured at the Chałupy station.

development of filter-feeders such as mussels Cerastoderma glaucum or Limecola balthica (Olenin and Daunys, 2005), which dominated the macrozoobenthos biomass in this region (Fig. 2b; Table SII). 3.3. Mercury concentration in macrozoobenthos The concentrations of total mercury (HgTOT) assayed in macrozoobenthic organisms collected in the coastal zone of Puck Lagoon in 2017 ranged from 12.4 to 58.7 ng g−1 (mean: 35.1 ng g−1) (Table SIII) and were close to the values recorded in benthic invertebrates collected in this area in 2015 by Wilman et al. (2019) (range: 14.2–74.1 ng g−1, mean: 26.9 ng g−1) and in 2016 by Jędruch et al. (2018a) (range: 17.0–111.0 ng g−1, mean: 38.0 ng g−1). Hg level in benthic macrofauna was about two times lower than measured in material collected in years 2012–2013 by Bełdowska et al. (2016b) and Jędruch et al. (2019b) (range: 4.1–252.0 ng g−1, mean: 62.9 ng g−1) and about five times lower compared to organisms sampled in 1995–1998 by Boszke et al. (2003a, 2003b) (range: 35.0–370.0 ng g−1, mean: 179.0 ng g−1). This indicates a downward trend in Hg concentration in the macrozoobenthos, which is most probably the environmental response to the reduction of Hg emissions and deposition since the 1990s (EMEP, 2016; KOBiZE, 2019). The concentrations of HgTOT in benthic macrofauna collected from research stations in Chałupy (mean: 34.5 ng g−1) and in Osłonino (35.6 ng g−1) did not differ statistically significant (p = 0.61) (Table SIII). However, there was spatial differentiation of HgTOT concentrations observed in the dietary components of macrofauna: sediments (p = 0.00), SPM (p = 0.00), macroalgae (p = 0.00), and vascular plants (p = 0.01). In all of these food sources, significantly higher concentrations of HgTOT were measured in the samples collected in Osłonino - in the case of sediments, the HgTOT level was more than two times higher than in Chałupy, in SPM it was about 70% higher, while in macroalgae and vascular plants the values were respectively 81% and 50% higher (Fig. 3; Table SIII). Elevated concentrations of HgTOT in these environmental components at the station in Osłonino had also been measured in earlier studies by the authors (Bełdowska et al., 2015; Bełdowska et al., 2016b; Jędruch et al., 2019b). A higher level of HgTOT in Osłonino station, compared to the station in Chałupy, was also measured in phyto- and zooplankton organisms (Bełdowska and Kobos, 2016; Bełdowska and Mudrak-Cegiołka, 2017), as well as in microphytobenthic algae - epilithon and epiphyton (Bełdowska et al., 2018b; Jędruch et al., 2019b). This was a consequence of increased surface runoff in the area of Osłonino, and hence a larger Hg load reaching the marine environment in this part of the lagoon (Bełdowska et al., 2016a; Jędruch et al., 2017; Kwasigroch et al., 2018). The quality and quantity of organic matter are important factors determining Hg concentration in benthic organisms (Jędruch et al., 2018a; Jędruch et al., 2019b). These factors also shape the availability of food for benthic fauna, which is particularly important, given the fact that Hg concentrations within one trophic level can be very different if the organisms have different feeding habits (Pempkowiak, 1997; Soto et al., 2011). In the case of the Chałupy station, elevated concentrations of HgTOT were recorded in the crustacean Idotea sp. (mean: 48.5 ng g−1) and the snail Peringia sp. (mean: 47.4 ng g−1) (Fig. 3). Both of these taxa belong to the organisms grazing on leaves and stems of benthic plants, but they can also feed on biofilm covering the macrophytes, consisting of bacteria and epiphytes (Kamermans et al., 2002; Riera, 2010). Although the concentration of HgTOT in vascular plants (mean: 5.2 ng g−1) collected in the Chałupy region was lower than in Osłonino (Fig. 3; Table SIII), the share of labile Hg fractions (mean: 94.1%) in Chałupy was larger (Fig. 4a). This was particularly true for Hg adsorbed on the leaf surface of vascular plants, available for grazers (Hg labile 1a), which accounted for up to one third (mean: 34.4%) of HgTOT. The fact that phytobenthos, together with the microorganisms that cover it, was an important source of Hg in the vicinity of the Chałupy station, is also evidenced by the elevated HgTOT concentration in another grazer:

3.4. Mercury accumulation in macrozoobenthos Only the Hg compounds occurring in the bioavailable form undergo accumulation in living organisms - they are mainly complexes with organic and inorganic ligands (Bradley et al., 2017). Hg compounds can adsorb on the surface of organisms, as well as penetrate into their interior (Pempkowiak, 1997). In the case of the Hg fractionation method used in this work, with regard to small organisms such as zoobenthos or elements of their diet, it can be assumed that Hg labile 1a is mainly adsorbed on the surface of organisms, and Hg labile 1b is absorbed inside the cells (Bełdowska et al., 2018a). In the case of the analysed zoobenthic organisms, it was found that the share of individual Hg fractions in their soft tissues depended on the study area (Fig. 4; Table SIV). 6

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Fig. 3. Mean ( ± SD) concentrations of total mercury (HgTOT) in the individual macrozoobenthos species and elements of their diet at research stations in the coastal zone of the Puck Lagoon (for details, see Table SIII).

The adsorption of Hg on the surface of macrofauna was largely conditioned by the morphological and physiological traits of the latter (Kuiper, 1981; Bełdowska and Kobos, 2016). The highest share of the adsorbed form of Hg (Hg labile 1a) (mean: 51%) was found in insect larvae (Fig. 4a). That was most probably associated with the considerable surface area of the larval skins produced around the larvae or individual parts of their bodies (Ruppert and Barnes, 1994). A high proportion of this Hg fraction was also observed in the polychaetes Marenzelleria sp. (mean: 50%) and Hediste diversicolor (average: 44%), whose various structural elements (chaetae, antennae, palps) favour Hg adsorption (Sikorski and Bick, 2004). In addition, these taxa, due to their ability to penetrate deeply into the sediment (up to 35 cm), adsorbed Hg bound with the fine sediment fraction on their surface (Żmudziński, 1996; Bonaglia et al., 2013). The proportion of adsorbed Hg (Hg labile 1a) in macrozoobenthos was significantly higher (p = 0.03) at the station in Osłonino (mean: 46.6%, range: 26.1–64.7%) compared to the station located in Chałupy (mean: 35.0%, range: 17.8–51.1%) (Table SIV). In addition, in the area of Osłonino, Hg labile 1a fraction dominated over other Hg fractions assayed in macrozoobenthos, while in Chałupy absorbed organic Hg (Hg labile 1b) was the fraction with the highest average share (mean: 59.3%, range: 28.1–80.1%) (Table SIV). The share of Hg labile 1b in macrofauna from Chałupy station was significantly higher (p = 0.02) than in Osłonino (mean: 43.0%, range: 21.6–60.6%). The predominant share of the Hg labile 1a fraction in Osłonino was most likely related to the environmental parameters of this station. The adsorption processes on the surface of organisms could be favoured by, e.g. the pH of the bottom water which is lower compared to Chałupy (Pempkowiak,

1997). However, the largest share of Hg labile 1a in benthic fauna in Osłonino was most probably associated with the limited transport of Hg into the cells. The accumulation of Hg-rich organic matter in the area of Osłonino was on one hand conducive to the increased Hg concentrations in organisms, but on the other hand also effective in deteriorating aerobic conditions in the bottom water and sediments, thus leading to decreased Hg bioavailability (Jędruch et al., 2018a). In the surface sediments collected in Osłonino, almost half of Hg (mean: 46.8%) occurred in the form of the stable HgS, inaccessible for organisms (Fig. 4b) - a compound characteristic of reductive conditions. In contrast, in Chałupy, where sediments were better oxygenated, the share of this fraction was much lower (mean: 34.0%) (Fig. 4a). The anaerobic conditions in sediments in the area of Osłonino (confirmed by negative Eh values) (Table SI), along with the periodically occurring H2S and the multiplication of anaerobic bacteria (Bełdowska et al., 2013; Jędruch et al., 2018a), also helped to limit Hg absorption in benthic organisms (Sokołowski, 2009; Wyn et al., 2009). This is evidenced by the share of the Hg labile 1b fraction in the macrozoobenthos in Osłonino being much lower than at the station in Chałupy (Table SIV). The limited accumulation of Hg from surface sediments in macrozoobenthos in the area of Osłonino is confirmed by the values of the BSAF coefficient. The values calculated for the station in Osłonino (mean: 13.2; range: 8.4–18.8) were less than half that observed at Chałupy station (mean: 31.4; range: 17.1–44.0) (p = 0.00) (Fig. SII). Although HgTOT concentrations in sediments in Osłonino were more than twice as high (Table SII), the total share of bioavailable labile Hg fraction (mean: 47.1%) (Fig. 4a) was smaller than in Chałupy (mean: 58.9%) (Fig. 4b). The Hg absorption in zoobenthic organisms could also 7

Marine Pollution Bulletin 153 (2020) 110968

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Fig. 4. Mean share of labile and stable Hg fractions in the individual macrozoobenthos species and elements of their diet in the coastal zone of Puck Lagoon at research stations in a) Chałupy and b) Osłonino (for details, see Table SIV).

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be related to the degree of primary production in the area of the research stations (Kidd et al., 2012). The greater load of nutrients in the area of Osłonino, associated with increased surface runoff, influenced the multiplication of micro- and macroalgae (Pickhardt et al., 2002). During blooms Hg was intensively accumulated in primary consumers as a consequence, due to the large biomass of algae, so-called dilution occurred, and the concentration of bioavailable Hg in individual algae cells was found to be low (Jędruch et al., 2019b).

4. Conclusion The results presented in this paper confirm that the surface run-off is an important determinant of the bioavailability and trophic transfer of Hg in the marine environment. The inflow of Hg from land lea to an increase in the Hg level in the food sources (sediments, suspended matter and primary producers), however, did not affect the Hg concentrations in the benthic fauna. It was related to the environmental conditions that occurred in the lagoon as a result of the intensive accumulation of organic matter in the coastal zone. The present study showed that oxygen deficit in the near-bottom zone, together with a decreased pH, limited the bioavailability of Hg in sediments and the uptake of labile Hg by benthic organisms. Increased primary production, stimulated by the inflow of biogenic salts favoured the biodilution of Hg in the growing biomass of plants. Elevated concentration of suspended matter and phytoplankton contributed to the increase of macrozoobenthic biomass and led to an intensified uptake of Hg adsorbed on organic particles by filter-feeders. The availability of food influenced the species composition and spatial distribution of zoobenthos - in the area covered with underwater meadows the biomass of fauna was dominated by grazers to which the main source of Hg were labile forms adsorbed on the surface of plants. Hg level was the highest in predatory organisms, occupying a higher trophic position than the suspensivorous and herbivorous species. The Hg biomagnification factor in Puck Lagoon in the summer season exceeded the global average, it was also about two times higher than the annual mean determined for the region. Also, the calculated Hg biomagnification factor was different depending the research station. Higher values were calculated for the marine-influenced area, where better oxygen conditions together with a higher pH promoted the uptake of mercury. The trophic transfer of Hg was favoured by the biomass of benthic fauna and large share of labile Hg forms in organisms. Importantly, the labile Hg forms constituted the predominant share of Hg in macrozoobenthos (90% on average). Due to the fact that benthic macrofauna is an essential component of the diets of fish, including those caught for consumption, as well as being increasingly consumed by humans, it can be an important source of Hg to the trophic chain.

3.5. Trophic transfer of mercury HgTOT concentrations assayed in particular taxa of macrozoobenthos in Puck Lagoon increased along with their trophic level (Fig. SIII; Table SV). The obtained results indicate that the HgTOT biomagnification potential (TMS), calculated for research stations in Puck Lagoon in the summer season, was 0.39. This value was higher than the values reported by other researchers for aquatic trophic webs (0.10–0.30) (Chen et al., 2000; Campbell et al., 2003; Lavoie et al., 2013), which means that the biomagnification of HgTOT in Puck Lagoon is exceptionally intense. The calculated TMS was also higher than that measured in this area by authors in previous years (0.22) (Jędruch et al., 2019b). This was due to the fact that the result was the average of results from the whole year, and not, as in the case of the present work, only from the summer season. Higher TMS in the summer can be explained by the increased level of Hg concentrations in the surrounding environment and in the food of zoobenthos (Bełdowska et al., 2016a; Bełdowska et al., 2018b; Jędruch et al., 2019b) compared to other months of the year, combined with relatively small biomass of organisms, observed in previous studies by the authors (Jędruch et al., 2018a). The more intensive Hg transfer in the summer could also have been affected by the hydrochemical conditions of the Puck Lagoon, such as salinity (Nowacki, 1993), which was lower than the annual mean, and the associated lower ion concentration (mainly Cl−, Na+, SO42−), affecting the reduction of Hg bioavailability (Jędruch et al., 2018a). Calculated on the basis of TMS, the biomagnification factor (BMF) of HgTOT for Puck Lagoon in the summer season was 3.79. This means that the Hg concentration increases almost 4 times in successive trophic levels. This value is more than twice as high as the global average (1.80) (Lavoie et al., 2013), which is most probably related to the relatively low productivity of the Puck Lagoon (compared to other water bodies), as well as to environmental conditions related to geographical latitude (Sokołowski, 2009; Sokołowski et al., 2012). The size of the HgTOT trophic transfer differed between the research stations in Chałupy and Osłonino. In the summer in Chałupy, TMS was 0.41 (p = 0.00), while in Osłonino it was 0.37 (p = 0.00) (Fig. SIII), and the calculated BMFs were 4.02 and 3.51, respectively. This means that Hg biomagnification in Chałupy is more intense than in Osłonino. A similar tendency was also noted in previous research by the authors - the BMF factor calculated for the whole year for the trophic web in Chałupy was at that time 40% higher than the BMF in Osłonino (Jędruch et al., 2019b). The more intensive biomagnification of Hg in Chałupy can be explained by better oxygenation of waters and sediments compared to the station in Osłonino, as well as by higher pH (Table SI), which is an important determinant of methylation of inorganic Hg forms and its bioavailability (Wyn et al., 2009; Jędruch et al., 2018a). This is confirmed by the share of individual Hg fractions - in Chałupy the total share of bioavailable, labile Hg in macrozoobenthos was higher than in Osłonino and amounted to as much as 95.5% (Table SIV; Fig. SII). Despite the fact that HgTOT concentrations in macrozoobenthos at the research stations were similar, and those for dietary components were higher in Osłonino (Table SIII), the trophic transfer of Hg in Chałupy was more effective. This was favoured by the macrofauna biomass there which was over two times lower than in Osłonino (Fig. 2b; Table SII), as well as by the lower biomass of primary producers (Bełdowska et al., 2016b; Bełdowska and Kobos, 2016). Those factors conditioned a faster Hg transfer through successive trophic links (Kidd et al., 2012).

CRediT authorship contribution statement Agnieszka Jędruch:Conceptualization, Methodology, Validation, Formal analysis, Investigation, Resources, Writing original draft, Writing - review & editing, Visualization, Project administration, Funding acquisition.Magdalena Bełdowska: Conceptualization, Methodology, Writing - original draft, Writing review & editing, Supervision. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements The research was as part of project No. 538-G235-B558-17, funded by the University of Gdańsk. The authors would like to thank Dr. Emilia Jankowska (Institute of Oceanology of the Polish Academy of Sciences) for help during sample collection. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marpolbul.2020.110968. 9

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