Science of the Total Environment 701 (2020) 134842

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Science of the Total Environment

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Operationally defined mercury (Hg) species can delineate Hg

bioaccumulation in mangrove sediment systems: A case study
Kartheek Chennuri a, Parthasarathi Chakraborty a,b,⇑, Saranya Jayachandran b, Sandip Kumar Mohakud a,
Ishita Ishita a, Darwin Ramteke a, Prasad Pramod Padalkar b, Prakash C. Babu a, Korupolu Raghu Babu c
a
Geological Oceanography Division, CSIR-National Institute of Oceanography, Dona Paula, Goa 403004, India
b
Centre for Oceans, Rivers, Atmosphere and Land Sciences, Indian Institute of Technology Kharagpur, Kharagpur, West Bengal 721302, India
c
Department of Engineering Chemistry, Andhra University, Visakhapatnam, Andhra Pradesh 530003, India

h i g h l i g h t s g r a p h i c a l a b s t r a c t

 Operationally defined Hg species in

sediment can delineate Hg
bioaccumulation.
+
 Organomercury complexes, MeHg
and labile Hg are bioavailable forms
of Hg.
 Sedimentary organo-Hg species
increased Hg bioaccumulation.
 Pirenella cingulata can be a good
bioindicator for Hg pollution.
 L-Cysteine is a suitable ligand to
estimate bioavailable Hg in mangrove
sediment.

a r t i c l e i n f o a b s t r a c t

Article history: This study investigated the linkage between mercury (Hg) speciation in the surficial sediments from a
Received 25 February 2019 mangrove ecosystem of the Zuari Estuary, west coast of India, with Hg bioaccumulation in gastropods
Received in revised form 26 September collected from the same area. Multiple operationally defined protocols and methods were used for deter-
2019
mination of Hg speciation study in the mangrove sediments. Moderately low concentrations of Hg were
Accepted 4 October 2019
Available online 28 October 2019
observed in the sediments, ranging from 37.3 ± 1.9 to 79.6 ± 4.0 mg/kg. Geochemical fractionation showed
that a significant part of sedimentary Hg was present within the structure of the sediment (residual frac-
Editor: Mae Sexauer Gustin tion) and not bioavailable. Non-residual Hg was primarily associated with oxidizable (sedimentary
organic matter (SOM) or sulfide) binding phase of the sediments, and ranged from 9.2 ± 0.3 to
Keywords: 78.5 ± 3.9 mg/kg. Concentration of methylmercury (MeHg) (a neurotoxin) in the sediments varied from
Hg fractionation 1.7 ± 0.1 to 4.4 ± 0.1 mg/kg. L-Cysteine, a suitable complexing ligand, extractable Hg concentration in
Sedimentary methylmercury the sediments ranged from 4.3 ± 0.1 to 15.9 ± 0.3 mg/kg. Statistical analysis suggested that MeHg was
Organo-Hg compounds adsorbed on Fe/Mn oxyhydroxide phases in the sediments. L-Cysteine was found to extract sedimentary
Hg bioaccumulation MeHg and thermodynamically less stable Hg-SOM complexes from the sediments. Concentrations of
Gastropod bioaccumulated Hg in soft tissues of the gastropod, Pirenella cingulata, ranged from 57.6 ± 4.4 to
Mangrove sediment
224.4 ± 7.2 mg/kg. Positive correlations existed between the concentration of bioaccumulated Hg in the
gastropods and the concentrations of Hg associated with the oxidizable phase, sedimentary MeHg and
L-Cysteine extracted Hg in the sediments. This study indicated that operationally defined Hg species
can be useful in estimating bioavailable Hg to obligatory deposit feeder in tropical mangrove systems.
Ó 2019 Elsevier B.V. All rights reserved.

⇑ Corresponding author at: Centre for Oceans, Rivers, Atmosphere and Land Sciences, Indian Institute of Technology Kharagpur, Kharagpur, West Bengal 721302, India.
E-mail address: [email protected] (P. Chakraborty).

https://doi.org/10.1016/j.scitotenv.2019.134842
0048-9697/Ó 2019 Elsevier B.V. All rights reserved.
2 K. Chennuri et al. / Science of the Total Environment 701 (2020) 134842

1. Introduction ation study, (2) extraction of sedimentary MeHg, and (3) L-cysteine
extractable sedimentary Hg. The information was used to assess
Distribution, flux, bioavailability, and toxicity of metals in natu- bioavailable Hg concentration in mangrove sediments.
ral/marine system depend on their chemical speciation (O’Donnel Gastropod species was chosen as a bio-indicator for estimating
et al., 1985; Prokop et al., 2003; Ansari et al., 2004; van Leeuwen Hg-bioaccumulation in this study. Cardoso et al (2013) have
et al., 2005; Benson et al., 2013; Chakraborty et al., 2010; reported that gastropod is a tolerant species to Hg. Berto et al.
Chakraborty, 2017). Various operationally defined protocols have (2006) reported that bioaccumulation of Hg in Nassarius reticulatus
been widely reported for metal speciation study in natural/marine (Gastropoda, Prosobranchia) gradually increases with increasing sed-
systems (Liang and Karamanos, 1993; Rauret et al., 1999; imentary Hg concentration in the southern Venice Lagoon. Aquatic
Ahnstrom and Parker, 2001; Bloom et al., 2003; Oyeyiola et al., gastropod has been identified as a good bioindicator of Hg pollution
2011; Jayachandran et al., 2018). However, there is no direct evi- in Pantanal of Poconé region (Mato Grosso, Brasil; Callil and Junk,
dence whether operationally defined metal species really estimate 2001). Pirenella cingulata (Family Potamididae), a common and
bioavailable fractions of the metal in an environment or not. In this widely available gastropod, was chosen as a bioindicator in this
study, different operationally defined protocols were used to speci- study. Pirenella cingulata has been reported to be abundantly found
ate sedimentary Hg (one of the high priority pollutants) and its in India, different parts of Southeast Asia, Vietnam (Zvonareva &
relation to Hg bioaccumulation in a tropical mangrove system. Kantor, 2016), Indonesia (Reid & Ozawa, 2016). It is also a dominant
Several operationally defined protocols have been widely used species in the intertidal and sub-tidal zones of estuarine mangrove
for Hg speciation study in marine/estuarine sediments systems of Goa coast, India (Sarkar et al., 1999). However, there is no
(Chakraborty et al, 2014a; Padalkar et al., 2019). Different geo- data available that establish the linkage between Hg speciation and
chemical fractionation protocols have been extensively used to Hg-bioaccumulation in tropical estuarine systems. In this work, Pir-
quantify distribution of Hg in different binding phases of sedi- enella cingulata was used as bio-indicator.
ments collected from diverse ecosystems (Chakraborty et al., The objective of this study was to test the hypothesis that, Hg
2014b; Chakraborty and Babu, 2015; Issaro et al., 2009). In general, speciation (determined by operationally defined protocols) in sed-
geochemical fractionation protocols enable us to separate and iments can be useful in estimating bioavailability and bioaccumu-
quantify (a) Hg in water soluble, carbornate/bicarbonate and lation in mangrove ecosystem. This study also aimed to identify
exchangeable forms; (b) Hg associated with reducible binding the factors that control Hg fractionation, speciation, and bioavail-
phases of sediment; (c) Hg complexed with oxidizing phases of ability in surface mangrove sediments.
sediment; and (d) Hg present within the structure of the sedi-
ments. Sedimentary Hg in the (a), (b) and (c) phases are called
non-residual Hg and Hg in the (d) is considered as residual Hg. A 2. Materials and methods
part of non-residual sedimentary Hg represents bioavailable Hg
pool in sediment systems (Baldi and Bargagli, 1982; John and 2.1. Study area and sample collection
Leventhal, 1995; Adekola et al., 2010; Chakraborty et al., 2014a).
However, residual Hg has been recognized as inert and non- Sediment and biological samples were simultaneously collected
bioavailable Hg-pool (Baldi and Bargagli, 1982; John and from intertidal mangrove region of the Zuari Estuary (Sancoale),
Leventhal, 1995; Adekola et al., 2010; Chakraborty et al., 2014a). Goa, West coast of India. Twelve sampling locations are presented
Boszke et al., (2006) have assessed mobility and bioavailability of in Fig. 1. Sampling was done in two different seasons. The sampling
sedimentary Hg by geochemical fractionation study in sediments was done in ST-1, ST-3, ST-5, ST-7, ST-9, and ST-11 during monsoon
from the Tsunami inundated coastal zone of Thailand. They also season (19th August 2015). The sediment and biological samples
used fractionation methods to assess mobility and bioavailability were also collected from ST-2, ST-4, ST-6, ST-8, ST-10, and ST-12
of Hg in soil from contaminated areas in Warshaw, Poland during post-monsoon period (04th November 2017). These sam-
(Boszke et al., 2008). They identified that water-soluble Hg and pling was purposefully done in two different seasons to check
acid-soluble Hg (exchangeable mercury) can easily enter aquatic whether operationally defined Hg speciation in mangrove sedi-
systems and accumulate in living organisms. Yu et al., (2012) and ments can delineate Hg bioaccumulation in sessile organisms or
Chakraborty et al (2015) have reported that SOM controls concen- not. Coordinates of the sampling locations are presented in the
tration, distribution, and lability of Hg in sediments. Bioavailability Supporting documents (Table 1).
of Hg has also been reported to control by MeHg concentration At low tide conditions, triplicate sediment cores were collected
(Ravichandran, 2004; Bergquist and Blum, 2007). Wang et al. at each station by using acid cleaned PVC pipe with a diameter of
(1998) reported that assimilation efficiencies (AE) for MeHg in bio- 7.5 cm. The sediment cores were brought back to the laboratory
logical system was much higher than Hg(II). MeHg displayed com- and stored at a temperature of 20 °C. Surface sediments (0–
parable AEs for both oxic and anoxic sediment. The uptake rate of 1 cm) of the three cores from each station were sub sectioned and
MeHg is much higher than Hg(II) species in marine environment. composite surface sediment was made by mixing these three sur-
There are several techniques and protocols that have been widely face sediments. Composite sediment samples were then freeze
used in literature to quantify MeHg in estuarine/marine sediments dried, subsequently ground milled, homogenized, and stored in
(Vazquez et al., 1997; Kehrig et al., 2003; Hammerschmidt and zip-lock bags at 4 °C. pH of overlying water column in the sampling
Fitzgerald, 2004). An independent solvent extraction protocol is stations were determined by using a portable multiparameters
also widely used for sedimentary MeHg speciation (Maggi et al., meter (Eutech cyberscan PCD 650 with ECFC7252203B pH elec-
2009). L-Cysteine has been reported as an effective binding ligand trode, Thermo Scientific). A large number of marine gastropods (Pir-
for Hg in biological systems (Aschner and Aschner, 1990; Giles enella cingulata) of similar size (length 17.2 ± 2.1 mm and width
et al., 2003; Rooney, 2007). However, there are very few data avail- 4.7 ± 0.8 mm) were collected from the same locations during the
able in the literature that describe operationally defined sedimen- sediment sampling. Gastropods were then depurated in natural
tary Hg species and its relation to bioaccumulation in benthic seawater filled aquaria at room temperature for 48 h in the labora-
organism in tropical estuarine systems. In this study, Hg species tory. Soft tissues were then taken out by using Teflon coated forceps
in sediments were quantified by following three different opera- without breaking the shell. Soft tissues were further washed
tionally defined extraction protocols viz., (1) geochemical fraction- homogenized, freeze dried and preserved in zip-lock bags at 4°C.
 K. Chennuri et al. / Science of the Total Environment 701 (2020) 134842 3

Fig. 1. Map of sampling location in the estuarine mangrove system of the Zuari River.

Table 1
Environmental parameters (pH, salinity and temperatures) of overlying water and concentration of total carbon (TC), total inorganic carbon (TIC), total organic carbon (TOC), total
nitrogen (TN), particle size and spectral slope parameters (Slope of spectral region and slope ratio) in the studied sediments from twelve sampling location of the mangrove area.

Station ID Month of sampling pH Salinity (psu) TC (%) TIC (%) TOC (%) TN (%) Molar C/N Particle size (%) S275-295 SR
Sand Silt + Clay
ST-1 August 7.3 14.2 3.0 0.1 2.9 0.2 21.9 5.6 94.4 0.041 4.1
ST-2 November 8.28 30.8 3.6 0.3 3.3 0.3 14.7 6.9 93.1 0.011 1.0
ST-3 August 7.5 13.8 2.4 0.4 2.0 0.1 20.0 3.7 96.3 0.034 3.4
ST-4 November 8.08 29.2 4.0 0.2 3.8 0.3 14.7 2.3 97.7 0.008 1.1
ST-5 August 7.3 14.1 3.7 0.3 3.4 0.2 19.6 6.4 93.6 0.026 2.6
ST-6 November 7.75 30.1 4.2 0.1 4.1 0.3 15.1 2.6 97.4 0.010 0.9
ST-7 August 7.6 14.6 3.1 0.1 3.0 0.2 20.1 4.1 95.9 0.038 3.8
ST-8 November 8.25 30.1 3.3 0.5 2.7 0.2 15.8 10.7 89.3 0.008 1.3
ST-9 August 7.6 15.0 4.0 0.1 3.9 0.2 21.2 4.1 95.9 0.024 2.7
ST-10 November 8.51 30.0 4.5 0.4 4.1 0.3 15.2 9.5 90.5 0.010 0.9
ST-11 August 7.5 14.5 4.1 0.7 3.4 0.2 26.6 3.3 96.7 0.038 3.8
ST-12 November 8.37 19.5 3.9 0.2 3.7 0.3 15.8 4.8 95.2 0.010 1.0

2.2. Texture analysis was extracted from the sediments by following the protocol
described by He et al. (2016). An approximate amount of 0.5 g of
A particle size analyzer (LPSA, Malvern Mastersizer 2000) was powdered sediment sample was mixed with 20 mL of 0.05 N
used to determine the grain size distribution in the studied sedi- sodium hydroxide (NaOH) solution and pH of the slurry adjusted
ments. Frozen sediment samples were dried at 50 °C in an oven to 10. The mixture was vertically shaken at 50 rpm for 12 h to
and wet sieved through <62 mm to separate sand fractions from extract SOM from the sediments. The mixture was then cen-
the bulk sediment. Silt and clay fractions were quantitatively deter- trifuged at ~3000 rpm for 10mins. SOM containing alkali extract
mined by using LPSA (Chakraborty et al., 2015; Ramaswamy and was then separated by slow decantation and used for spectropho-
Rao, 2006). Standard particles of 0.2–62 mm sizes (viz., Duke’s latex tometric characterization of SOM. Absorbance of SOM was mea-
and glass sphere standards) were used to calibrate the instrument. sured at wavelengths ranging from 200 to 700 nm. Spectral
Each sample was analyzed three times and the mean was calculated. absorbance at 250, 364, 465, and 665 nm were used to calculate
the E2/E3, E4/E6 ratios as described in the literature (Chen et al.,
2.3. TOC/TIC/TN analysis 1977; Helms et al., 2008). Accuracy and precision of the spec-
trophotometer was repeatedly checked by using NIST-grey glass
Concentrations of total carbon (TC), and total nitrogen (TN) in filters SRM 1930 and Holmiumoxide Solution (Merck reference
the sediment were determined by using Flash 2000 CHN- material for SpectroquantÒ PhotoCheck) (Travis, et al., 2005).
Elemental Analyzer (Thermo Fisher Scientific Incorporation) with
a precision of ±5%. Soil NC from Elemental Microanalysis Ltd, UK 2.5. Determination of total mercury (HgT) in the sediments and
(Cat No B2051) was used as certified reference material. Total inor- biological samples
ganic carbon (TIC) was determined by using coulometer (UIC
Coulometrics). Anhydrated calcium carbonate was used as certified Concentrations of Hg in sediments and biological samples were
reference material (99.5% pure, Merck, Germany). Sedimentary determined by using direct mercury analyzer (Tri-Cell DMA–80,
organic matter (SOM) was calculated by subtracting TIC from TC. Milestone, Italy). The working principle of DMA-80 is based on fol-
lowing steps: (a) thermal decomposition of sample, (b) catalytic
2.4. Spectrophotometric characterization of SOM conversion and removal of interfering species, (c) pre-
concentration of Hg in gold by amalgamation and (d) determina-
Molecular characterization of SOM was done by using UV–Vis- tion of Hg by atomic absorption spectrophotometry. Oxygen was
ible Spectrophotometer (Merck, Spectroquant Pharo 300). SOM used as the carrier gas in DMA-80. MESS-3 and PACS-2 were the
4 K. Chennuri et al. / Science of the Total Environment 701 (2020) 134842

certified reference materials (CRM) used to check the sensitivity 3. Results and Discussion
and recovery of the instrument. The analysis of certified Hg con-
centrations in the MESS-3 and PACS-2 were found to be Variation in pH (ranging from 7.30 ± 0.05 to 8.51 ± 0.05) and
91.0 ± 9.0 and 3020.0 ± 100 mg/kg, respectively. DORM-4 (fish pro- salinity (ranging from 13.8 to 30.8 PSU) of overlying water in the
tein, a CRM used for trace metal analysis, from National Research sediment sampling stations represents the two sampling seasons
Council Canada) was used to check Hg recoveries from the soft tis- (Table 1). Freshwater dominated monsoon was reflected by the
sues of the gastropod. The certified concentration of Hg in DORM-4 low pH and salinity, and post-monsoon season represented by high
was 412.0 ± 36.0 mg/kg. Total recovery percentage of Hg from the pH and salinity. Sediments samples were dominated by finer par-
CRM’s were more than 99%. The data are expressed as aver- ticles (>95%) at all the twelve stations in both the seasons. Concen-
age ± standard deviation (n = 3) for Hg. Detection limit of DMA- tration of SOM varied from 2.0 to 4.1% (wt%). Total sedimentary
80 is 0.02 ng of Hg. nitrogen (TN) concentration ranged from 0.14 to 0.22 (wt%). A pos-
itive correlation (r2 = 0.6, p < 0.05) between the SOM and TN (as
2.6. Sequential extraction protocol for geochemical fractionation of shown in Supporting material Fig. 4SM) suggests that sedimentary
sedimentary Hg TN were primarily associated with the SOM. C/N ratio of the SOM
varied from 14.7 to 26.6, indicating of their terrestrial origin and
The sequential extraction protocol suggested by the European non-labile nature (Chakraborty et al., 2015, 2016) during the sam-
Community Bureau of Reference (Rauret et al., 1999) was applied pling times.
to quantify Hg distribution in different binding phases of the stud- UV–Visible spectrophotometer was used to qualitatively char-
ied sediments. The sequential extraction protocol helped to esti- acterize the SOM. Spectral slope coefficient of the SOM between
mate the concentrations of (1) water soluble and carbonate/ 275 nm and 295 nm (S275–295) and ratio of the spectral slope coef-
bicarbonate form of Hg (Fr1), (2) Hg associated with Fe-Mn oxyhy- ficients (SR = S275–295/S350–400) provided qualitative information
droxides (Fr2), (3) Hg associated with organic matter and sulfide about molecular weight (MW) of the SOM in the studied
(Fr3) and (4) Hg within the structure of the sediment (Fr4). The sediments.
detail description of the protocol is presented as Supporting mate- S275–295 and SR of the SOM varied from 0.008 to 0.041 and 0.9–
rial Fig. 1SM. The non-residual Hg fractions (Fr1 + Fr2 + Fr3) are 4.1 respectively (Table 1). Both S275–295 and SR values are inversely
grossly considered as labile Hg complexes in sediments. It is related with the MW of the SOM. The MW of the SOM was found to
important to note that total sedimentary Hg concentration and depend on the pH and salinity of the overlying bottom water
the sum of the concentration of Hg associated with different bind- (Fig. 5SM). Fig. 5SM shows that SR value of the SOM exponentially
ing phases were compared to evaluate the quality of our data. BCR- decreased with increasing pH and salinity of the overlying water
701 was used as a CRM to assess the accuracy of extraction proto- column, and indicates an increase in MW of SOM with pH and
col. Many other protocols has also been used for sedimentary Hg salinity. However, it is difficult to correlate the MW of SOM with
fractionation in the literature (Bloom et al., 2003; Renneberg and pH and salinity as there are many other factors (such as supply
Dudas, 2001; Wallschläger et al., 1996). However, the BCR protocol of terrestrial organic matter, land runoff, bacterial activity, and
had been successfully used in our previous studies (Chakraborty local hydrodynamics) that can affect the system. It is just sug-
et al., 2014a,b) and therefore, further applied in this study. gested that the MW of SOM changed in two different sampling
seasons.
Sedimentary Hg concentrations varied from 37.3 ± 1.9 to
2.7. Determination of sedimentary methylmercury (MeHg)
79.6 ± 4.0 mg/kg. Based on the sediment quality guidelines devel-
oped for the National Status and Trends Program, this sediment
The protocol, used for methylmercury (MeHg) extraction from
samples can be classified as uncontaminated sediment with
sediment in this study, has been described in the literature
respect to total Hg concentration and safe for environment and
(Chakraborty et al., 2016; Maggi et al., 2009). The flow chart of
human health (NOAA, 1999).
the protocol is presented as Supporting material Fig. 2SM. The cer-
Positive linear correlation (r2 = 0.5, p < 0.05) existed between
tified reference material of MeHg from Sigma-Aldrich (SQC1238)
the total Hg and SOM concentrations (Fig. 6SM) in the sediments
was used to check the sensitivity of the extraction prtotocol. The
at two different seasons. This observation indicates that SOM in
certified value of MeHg was 10.00 ± 0.35 mg/kg. The recovery of
the sediments probably acted as a host for Hg. It has been reported
MeHg from the CRM was more than 97%.
in the literature that SOM act as a host for Hg in estuarine and
mangrove sediments (Chakraborty et al., 2014a). However, no sig-
2.8. Determination of L-cysteine extractable sedimentary Hg nificant relationship was observed between varying C/N ratio
(ranging from 14.7 to 26.6) and total Hg concentration in the sed-
L-cysteine, an essential amino acid, present in different types of
iments. This observation suggests that variation in non-lability
organisms, in natural and marine systems, has been used as a suit- (represented by changing C/N ratio) of SOM did not have influence
able complexing ligand for Hg (Maggi et al., 2009) in natural sys- on sedimentary Hg concentration. In order to understand distribu-
tem. In this study, L-cysteine was used as an extractant to release tion, fate, and bioavailability of sedimentary Hg, three independent
leachable Hg (i.e. thermodynamically weak Hg complexes) from operationally defined extraction protocols were carried out in the
the sediments. This extraction was done to mimic the ligand studied sediments.
exchange reaction which probably occurs in biological systems.
The detail description of the extraction protocol is presented as
Supporting material Fig. 3SM. 3.1. Geochemical fractionation of Hg in mangrove sediments

2.9. Quality control/quality assurance (QA/QC) Table 2 shows that Hg had different affinity towards different
binding phases of the sediments. Concentration of water soluble,
USEPA (QA/QC) protocols (Barron et al., 1995) were closely fol- exchangeable, and carbonate and bicarbonate forms (Fr1) of Hg
lowed during analyzing sediment and biological samples, running were not detectable (<LOD of DMA-80) in the sediments. Hg con-
triplicate samples and blanks. The direct mercury analysis follows centration in reducible phase (i.e. with the Fe/Mn-oxyhydroxy
USEPA Method 7473. phase, Fr2) of the sediments varied from very low (not detectable)
 K. Chennuri et al. / Science of the Total Environment 701 (2020) 134842 5

Table 2
Distribution of total Hg (HgT), and operationally defined Hg species, such as, Hg in different binding phases of sediments (by geochemical fractionation study), concentration of
MeHg, concentration of L-Cysteine extracted Hg in sediments and Hg bioaccumulation in gastropod.

Station Total Hg (mg/ Fr 1 + Fr 2 Fr 3 (%) Fr 4 (%) 5% L-Cysteine extracted Hg (mg/ MeHg (mg/ MeHg in Total Hg Hg from gastropod (mg/
ID kg) (%) kg) kg) (%) kg)
ST-1 44.2 ± 2.2 27.3 ± 1.4 54.8 ± 2.7 17.9 ± 0.9 12.6 ± 0.3 3.5 ± 0.1 7.9 156.8 ± 5.4 (n = 200)
ST-2 59.9 ± 3.0 4.4 ± 0.1 10.9 ± 0.3 84.7 ± 2.5 8.8 ± 0.2 3.1 ± 0.1 5.1 131.0 ± 3.9 (n = 160)
ST-3 37.3 ± 1.9 n.d. 75.6 ± 3.8 24.4 ± 1.2 12.6 ± 0.3 3.4 ± 0.1 9.0 224.4 ± 7.2 (n = 200)
ST-4 70.9 ± 3.5 9.2 ± 0.3 9.2 ± 0.3 81.6 ± 2.4 12.4 ± 0.2 3.0 ± 0.1 4.3 138.0 ± 4.1 (n = 160)
ST-5 63.4 ± 3.2 12.3 ± 0.6 35.0 ± 1.8 52.6 ± 2.6 14.5 ± 0.3 4.4 ± 0.1 7.0 128.8 ± 4.8 (n = 200)
ST-6 79.6 ± 4.0 7.0 ± 0.2 13.0 ± 0.4 80.0 ± 2.4 12.5 ± 0.2 2.7 ± 0.1 3.4 159.0 ± 4.8 (n = 160)
ST-7 43.3 ± 2.2 n.d. 78.5 ± 3.9 21.5 ± 1.1 11.4 ± 0.2 3.0 ± 0.1 6.9 184.6 ± 1.8 (n = 200)
ST-8 56.9 ± 2.8 5.4 ± 0.2 11.4 ± 0.3 83.3 ± 2.5 13.3 ± 0.1 2.8 ± 0.1 4.9 69.0 ± 2.1 (n = 160)
ST-9 47.4 ± 2.4 n.d. 32.7 ± 1.6 67.3 ± 3.4 4.3 ± 0.1 1.7 ± 0.1 3.5 57.6 ± 4.4 (n = 200)
ST-10 57.9 ± 2.9 6.4 ± 0.2 11.8 ± 0.4 81.7 ± 2.5 10.9 ± 0.2 2.1 ± 0.1 3.7 74.0 ± 2.2 (n = 160)
ST-11 52.4 ± 2.6 10.7 ± 0.5 58.3 ± 2.9 31.1 ± 1.6 11.6 ± 0.2 2.9 ± 0.1 5.5 111.4 ± 3.7 (n = 200)
ST-12 72.6 ± 3.6 5.1 ± 0.2 11.6 ± 0.3 83.4 ± 2.5 15.9 ± 0.3 1.8 ± 0.1 2.5 108.0 ± 3.2 (n = 160)

to 27.3 ± 1.4 mg/kg (~0–27% of the total sedimentary Hg concentra- (Fig. 2b). However, weak correlation was observed between the
tion). Concentrations of Hg associated with oxidizable phase (i.e. Hg loading and Hg association with the reducible phase. Geochem-
with SOM and sulphide binding phases in the sediments, Fr3) of ical fractionation data of Hg suggests that organomercury com-
the sediment ranged from 9.2 ± 0.3 to 78.5 ± 3.9 mg/kg (~9.2% to pounds were predominant in the non-residual Hg in the
75.6% of the total Hg content in the sediments). A major part of sediments. Therefore, further operationally defined protocol was
the total sedimentary Hg (17.9–84.7% of the total Hg) was present used to estimate sedimentary MeHg concentration.
within the structure (residual fraction, Fr4) of the sediments. Con-
centration of Hg in the residual fraction of the sediments is consid- 3.2. Methylmercury (MeHg) in mangrove sediments
ered as inert and non-bioavailable Hg (Fig. 2a).
A negative correlation (r2 = 0.6, p < 0.05) was observed between The concentrations of MeHg in the studied sediment varied
the concentration of Hg associated with the oxidizable phase and from 1.7 ± 0.1 to 4.4 ± 0.1 lg/kg. Fig. 3a showed that a negative cor-
total sedimentary Hg concentration in the sediments (Fig. 2b). This relation existed between the concentrations of MeHg and SOM in
negative relationship can be explained by considering the com- the sediments (r2 = 0.7, p < 0.05). This observation can be justified
plexation and reduction reactions of Hg with SOM in the sedi- by considering the C/N ratio of the SOM. It has been reported that
ments. Complexation (i.e., association of Hg with oxidizable labile SOM (C/N = 4–10) increases MeHg formation in marine sed-
phase) probably predominated over Hg reduction reaction at low iments (Chakraborty et al., 2015; Schartup et al., 2015). The pres-
Hg loading in the sediments, but reduction processes gradually ence of inert SOM (with C/N > 11) in the studied sediment
increased with increasing Hg loading in the sediment. It has been increased reduction/complexation of Hg(II) and decreased MeHg
reported in the literature that Hg-dissolved organic carbon (DOC) formation. C/N ratio of the SOM in the studied sediments indicated
complexation predominates at lower Hg loading, but reduction their terrestrial origin and non-labile nature and, therefore, did not
reaction predominates at higher Hg concentration (Chakraborty promote MeHg formation in the system.
et al., 2016). Phenolic-OH and –COOH groups in DOC have been Fig. 3b also shows that negative correlation existed between
reported to interact with Hg(II) and favor photoreduction of Hg total sedimentary Hg concentrations and MeHg concentrations
(II) (Fantozzi et al., 2007). Data collected in this study suggested (r2 = 0.5, p < 0.05) in the sediments. Both these observations indi-
that increasing Hg concentrations in the sediments decreased Hg cate that SOM plays important role in complexing Hg and control-
association with SOM, and increased Hg reduction process and ling MeHg formation in the sediment system. It is proposed that Hg
Hg concentration in the reducible phase of the sediments reduction (at higher Hg loading in the sediment) decreased MeHg

Fig. 2. (a) Distribution of Hg (%) in different binding phases of the studied sediments. (b) Variation in the percentage of Hg associated with oxidizable phase with respect to
total sedimentary mercury concentration (mg/kg).
6 K. Chennuri et al. / Science of the Total Environment 701 (2020) 134842

Fig. 3. Variation in MeHg concentration (mg/kg) as a function of varying a) SOM (%) and b) HgT (mg/kg) in the studied mangrove sediments.

formation in presence of non-labile SOM (Chakraborty et al., 2015, in the solution. Concentration of extracted Hg was found to
2016; Vudamala et al., 2017). Thermodynamically weak Hg- increase with increasing L-cysteine concentration in the solution.
sediment complexes can be useful in providing better understand- The highest concentration of L-cysteine (5%) was used in this study.
ing fate, mobility and bioavailability of Hg in the sediments. Thus, However, further experiments are required to quantify optimized
another operationally define protocol used to estimate loosely L-cysteine concentration to extract bioavailable Hg (for a specific
bound Hg in the sediments. indicator species) from estuarine systems. The extracted Hg con-
centrations, in the sediments varied from 4.3 ± 0.1 to
3.3. Extraction of sedimentary Hg by L-cysteine 15.9 ± 0.3 mg/kg as shown in Table 2.
Combination of speciation data obtained from the above three
L-cysteine was used as a suitable competing ligand (with different operationally defined protocols suggests that Hg formed
respect to the other natural ligands) to leach out thermodynami- strong complexes with SOM at low Hg loading, but reduction pre-
cally less stable Hg complexes (with respect to the stability of dominated at higher Hg loading. There was a positive relationship
Hg-L-cysteine complexes) to estimate an approximate amount of existed between the Hg associated with the reducible fractions
bioavailable Hg in the sediments. The concentration of L-cysteine (r2 = 0.6, p < 0.05) and MeHg concentrations in the sediments
varied from 0.25% to 5% solution. The concentration of extracted (Fig. 4a). This observation indicated that a fraction of MeHg might
Hg was found to increase with increasing L-cysteine concentration have strongly adsorbed on the Fe/Mn oxyhydroxide phases in the

Fig. 4. (a) Variation in concentration of reducible Hg (mg/kg) fraction in the sediment with varying sedimentary MeHg concentration (with respect to the HgT) and (b)
Variation of sedimentary MeHg concentration with L-cysteine extractable Hg of the sediment.
 K. Chennuri et al. / Science of the Total Environment 701 (2020) 134842 7

Fig. 5. Variation in bioaccumulated Hg (mg/kg) concentrations in gastropod with varying (a) Percentage of Hg associated within the organic fraction of the sediment (b)
percentage of sedimentary MeHg (with respect to the total Hg) and (c) concentration of Hg leached by 5% solution of L-Cysteine.

sediments. It has been reported in the literature that Hg and MeHg Taylor et al., (2012) observed an increase in Hg-bioaccumulation
strongly adsorb onto iron oxyhydroxide over the pH range of 3.2– with increasing total sedimentary Hg concentration in a southern
7.1 (Rytuba, 2000). It has been reported that iron oxide exhibits a New England estuary. Further, speciation parameters of sedimen-
strong adsorption and co-precipitation reaction with MeHg tary Hg were correlated with the bioaccumulated Hg concentration
(Feyte et al., 2010). Concentration of L-cysteine extractable Hg in the sediment system. Fig. 5a shows that there was a positive cor-
showed a positive relationship with MeHg concentration (r2 = 0.6, relation (r2 = 0.5, p < 0.05) existed between the fraction of total
p < 0.05) in the sediments (Fig. 4b). This observation suggests that sedimentary Hg associated with the oxidizable phase and the con-
L-cysteine extracted sedimentary MeHg from the sediment. It is centration of bio-accumulated Hg. This suggests that a fraction of
interesting to note that concentration of L-cysteine extractable Hg associated with oxidizable phase in the sediments were proba-
Hg was higher than MeHg concentrations in the sediments. This bly responsible for bioaccumulation of Hg in soft tissues of the
observation suggests that L-cysteine extracted not only MeHg from gastropods.
the sediments, but also thermodynamically less stable Hg-SOM Fig. 5b shows that bioaccumulation of Hg in the gastropods pos-
complexes (with respect to the stability of Hg-L-cysteine com- itively correlated (r2 = 0.6, p < 0.05) with the fraction of MeHg
plexes) from the sediments. Operationally defined Hg-speciation (with respect to total sedimentary Hg concentration) present in
data were further correlated with bioaccumulated Hg in the man- the sediments. Increasing concentration of sedimentary MeHg
grove system. (one of the highly toxic and bioavailable forms of Hg) increased
bioaccumulation of Hg in the gastropods. A similar relationship
has been reported in the literature (Désy et al., 2000).Fig. 5c also
3.4. Bioaccumulated Hg in gastropods (Pirenella cingulata) and its shows that a positive correlation (r2 = 0.7, p < 0.05) existed
relationship with operationally defined sedimentary Hg species between the fraction of total Hg extracted by L-cysteine and the
bioaccumulated Hg in the mangrove system. This observation sug-
Concentrations of bio-accumulated Hg in soft tissues of the gas- gest that concentrations of Hg associated with oxidizable phase,
tropods (Pirenella cingulata) varied from 57.6 ± 4.4 to sedimentary MeHg, and L-cysteine extractable Hg (from mangrove
224.4 ± 7.2 mg/kg. Variation in concentration of bioaccumulated sediment) are representative of bioavailable Hg in mangrove sedi-
Hg in the gastropods is presented in Table 2. Bioaccumulated Hg ment systems.
concentration in this region was very similar to the bioaccumu-
lated Hg concentrations reported from different unpolluted regions
of the world (57.6–224.4 mg/kg) (Levasseur, 1977; Metcalfe-Smith 4. Conclusions
and Green, 1992).
A weak correlation was found between the total sedimentary Overall, Hg associated with SOM, sedimentary MeHg, and L-
Hg concentration and the bioaccumulated Hg in the Pirenella cingu- cysteine extractable Hg in sediments was bioavailable for an obli-
lata species (Table 2). Weak relationship between total sedimen- gatory deposit feeder in the tropical mangrove systems in different
tary Hg concentrations and bioaccumulated Hg concentration, as seasons. A linkage was established between sedimentary Hg speci-
found in this study, suggests that total sedimentary Hg concentra- ation (by applying operationally defined protocols) and its bioaccu-
tion did not provide any information about bioavailability in the mulation in a sessile organism (Pirenella cingulate) in a tropical
sediment systems. However, positive correlation between total mangrove system. However, this biological species cannot be used
sedimentary Hg concentrations and bioaccumulated Hg in the ben- as an indicator to reflect the status or predict the condition(s) (with
thic organisms has been reported in the literature (Hornung et al., respect to Hg) of mangrove environments. It is important to note
1981). Berto et al. (2006) reported that a positive correlation that establishing a relationship between sedimentary Hg specia-
between HgT concentration in sediments and bioaccumulated Hg tion with bioaccumulation in a single population rarely reflects
in the gastropod (N. reticulatus) from the southern Venice Lagoon. the complexity of an environment. Therefore, further research is
8 K. Chennuri et al. / Science of the Total Environment 701 (2020) 134842

needed to prove whether operationally defined Hg speciation in Chakraborty, P., Babu, P.R., Vudamala, K., Ramteke, D., Chennuri, K., 2014a. Mercury
speciation in coastal sediments from the central east coast of India by modified
sediments can be holistically useful in delineating Hg bioaccumu-
BCR method. Mar. Pollut. Bull. 81 (1), 282–288.
lation in different biological species from tropical estuarine sys- Chakraborty, P., Babu, P.R., 2015. Environmental controls on the speciation and
tems or not. distribution of mercury in surface sediments of a tropical estuary, India. Mar.
Pollut. Bull. 95, 350–357.
Chakraborty, P., Sarkar, A., Vudamala, K., Naik, R., Nath, B.N., 2015. Organic matter—
Declaration of Competing Interest a key factor in controlling mercury distribution in estuarine sediment. Mar.
Chem. 173, 302–309.
Chakraborty, P., Sharma, B., Babu, P.R., Yao, K.M., Jaychandran, S., 2014b. Impact of
The authors declare that they have no known competing finan- total organic carbon (in sediments) and dissolved organic carbon (in overlying
cial interests or personal relationships that could have appeared water column) on Hg sequestration by coastal sediments from the central east
coast of India. Mar. Pollut. Bull. 79 (1–2), 342–347.
to influence the work reported in this paper. Chakraborty, P., Mason, R.P., Jayachandran, S., Vudamala, K., Armoury, K., Sarkar, A.,
Chakraborty, S., Bardhan, P., Naik, R., 2016. Effects of bottom water oxygen
concentrations on mercury distribution and speciation in sediments below the
Acknowledgements oxygen minimum zone of the Arabian Sea. Mar. Chem. 186, 24–32.
Chen, Y., Senesi, N., Schnitzer, M., 1977. Information provided on humic substances
by E4/E6 ratios 1. Soil Sci. Soc. Am. J. 41 (2), 352–358.
Authors are thankful to the Director, NIO, Goa, for his encour- Désy, J.C., Archambault, J.F., Pinel-Alloul, B., Hubert, J., Campbell, P.G., 2000.
agement and support. This work is a part of the Council of Scientific Relationships between total mercury in sediments and methyl mercury in the
and Industrial Research (CSIR)-NIO supported OLP1712 project. freshwater gastropod prosobranch Bithynia tentaculata in the St. Lawrence
River, Quebec. Can. J. Fish. Aquat. Sci. 57 (S1), 164–173.
This article bears NIO contribution number 6467.
Fantozzi, L., Ferrara, R., Frontini, F.P., Dini, F., 2007. Factors influencing the daily
behaviour of dissolved gaseous mercury concentration in the Mediterranean
Sea. Mar. Chem. 107 (1), 4–12.
Appendix A. Supplementary data Feyte, S., Tessier, A., Gobeil, C., Cossa, D., 2010. In situ adsorption of mercury,
methylmercury and other elements by iron oxyhydroxides and organic matter
in lake sediments. Appl. Geochem. 25 (7), 984–995.
Supplementary data to this article can be found online at Giles, N.M., Watts, A.B., Giles, G.I., Fry, F.H., Littlechild, J.A., Jacob, C., 2003. Metal and
https://doi.org/10.1016/j.scitotenv.2019.134842. redox modulation of cysteine protein function. Chem. Biol. 10 (8), 677–693.
Hammerschmidt, C.R., Fitzgerald, W.F., 2004. Geochemical controls on the
production and distribution of methylmercury in near-shore marine
References sediments. Environ. Sci. Technol. 38 (5), 1487–1495.
He, W., Lee, J.H., Hur, J., 2016. Anthropogenic signature of sediment organic matter
probed by UV–Visible and fluorescence spectroscopy and the association with
Adekola, F.A., Abdus-Salam, N., Bale, R.B., Oladeji, I.O., 2010. Sequential extraction of
heavy metal enrichment. Chemosphere 150, 184–193.
trace metals and particle size distribution studies of Kainji Lake sediment,
Helms, J.R., Stubbins, A., Ritchie, J.D., Minor, E.C., Kieber, D.J., Mopper, K., 2008.
Nigeria. Chem. Spec. Bioavail. 22 (1), 43–49.
Absorption spectral slopes and slope ratios as indicators of molecular weight,
Ahnstrom, Z.A.S., Parker, D.R., 2001. Cadmium reactivity in metalcontaminated soils
source, and photobleaching of chromophoric dissolved organic matter. Limnol.
using a coupled stable isotope dilutionsequential extraction procedure. Environ.
Oceanogr. 53 (3), 955–969.
Sci. Technol. 35, 121–126.
Hornung, H., Raviv, D., Krumgalz, B.S., 1981. The occurrence of mercury in marine
Ansari, T.M., Marr, I.L., Tariq, N., 2004. Heavy metals in marine pollution
algae and some gastropod molluscs of the Mediterranean shoreline of Israel.
perspective—a mini review. J. Appl. Sci. 4 (1), 1–20.
Mar. Pollut. Bull. 12 (11), 387–390.
Aschner, M., Aschner, J.L., 1990. Mercury neurotoxicity: mechanisms of blood-brain
Issaro, N., Abi-Ghanem, C., Bermond, A., 2009. Fractionation studies of mercury in
barrier transport. Neurosci. Biobehav. Rev. 14 (2), 169–176.
soils and sediments: a review of the chemical reagents used for mercury
Baldi, F., Bargagli, R., 1982. Chemical leaching and specific surface area
extraction. Anal. Chim. Acta 631 (1), 1–12.
measurements of marine sediments in the evaluation of mercury
Jayachandran, S., Chakraborty, P., Ramteke, D., Chennuri, K., Chakraborty, S., 2018.
contamination near cinnabar deposits. Mar. Environ. Res. 6 (1), 69–82.
Effect of pH on transport and transformation of Cu-sediment complexes in
Barron, J., Boone, P., Cantor-McKinney, S., Chase, T., Cotter, P., Dixon, T., Engler, B.,
mangrove systems. Mar. Pollut. Bull. 133, 920–929.
Fox, R., Fox, C., Graves, B., 1995. QA/QC Guidance for Sampling and Analysis of
John, D.A., Leventhal, J.S., 1995 Descargado de http://www.unalmed.edu.co/
Sediments, Water, and Tissues for Dredged Material Evaluations: Chemical
rrodriguez/MODELOS/depositos-ambiente/BioaviabilityOf Metal.pdf/el. In:
Evaluations (No. EPA-823-B-95-001). Environmental Protection Agency,
Bioavailability of Metals, p. 17.
Washington Dc Office of Water.
Kehrig, H.A., Pinto, F.N., Moreira, I., Malm, O., 2003. Heavy metals and
Benson, N.U., Anake, W.U., Olanrewaju, I.O., 2013. Analytical relevance of trace
methylmercury in a tropical coastal estuary and a mangrove in Brazil. Org.
metal speciation in environmental and biophysicochemical systems. Am. J.
Geochem. 34 (5), 661–669.
Anal. Chem. 4, 633–641.
Liang, J., Karamanos, R.E., 1993. DTPA-extractable Fe, Mn, Cu, and Zn. In: Carter, M.R.
Bergquist, B.A., Blum, J.D., 2007. Mass-dependent and-independent fractionation of
(Ed.), Soil Sampling and Methods of Analysis. CRC Press, Boca Raton, FL, pp. 87–
Hg isotopes by photoreduction in aquatic systems. Science 318 (5849), 417–
90.
420.
Levasseur, H., 1977. Étude du benthos du fleuve Saint-Laurent. Rapp. tech. no. 10.
Berto, D., Giani, M., Covelli, S., Boscolo, R., Cornello, M., Macchia, S., Massironi, M.,
Comité d’étude sur le fleuve Saint-Laurent et Service de protection de
2006. Mercury in sediments and Nassarius reticulatus (Gastropoda
l’environnement. Environnement Canada, Québec.
Prosobranchia) in the southern Venice Lagoon. Sci. Total Environ. 368 (1),
Maggi, C., Berducci, M.T., Bianchi, J., Giani, M., Campanella, L., 2009. Methylmercury
298–305.
determination in marine sediment and organisms by Direct Mercury Analyser.
Bloom, N.S., Preus, E., Katon, J., Hiltner, M., 2003. Selective extractions to assess the
Anal. Chim. Acta 641 (1–2), 32–36.
biogeochemically relevant fractionation of inorganic mercury in sediments and
Metcalfe-Smith, J.L., Green, R.H., 1992. Ageing studies on three species of freshwater
soils. Anal. Chim. Acta 479 (2), 233–248.
mussels from a metal-polluted watershed in Nova Scotia, Canada. Can. J. Zool.
Boszke, L., Kowalski, A., Astel, A., Barański, A., Gworek, B., Siepak, J., 2008. Mercury
70 (7), 1284–1291.
mobility and bioavailability in soil from contaminated area. Environ. Geol. 55
O’Donnel, J.R., Kaplan, B.M., Allen, H.E., 1985. Bioavailability of trace metals in
(5), 1075–1087.
natural waters. Aquatic Toxicology and Hazard Assessment: Seventh
Boszke, L., Kowalski, A., Szczuciński, W., Rachlewicz, G., Lorenc, S., Siepak, J., 2006.
Symposium. American Society for Testing and Materials, Philadelphia, PA.
Assessment of mercury mobility and bioavailability by fractionation method in
Oyeyiola, A.O., Olayinka, K.O., Alo, B.I., 2011. Comparison of three sequential
sediments from coastal zone inundated by the 26 December 2004 tsunami in
extraction protocols for the fractionation of potentially toxic metals in coastal
Thailand. Environ. Geol. 51 (4), 527–536.
sediments. Environ. Monit. Assess. 172 (1–4), 319–327.
Callil, C.T., Junk, W.J., 2001. Aquatic Gastropods as Mercury Indicatorsin the
Padalkar, P.P., Chakraborty, P., Chennuri, K., Jayachandran, S., Sitlhou, L., Nanajkar,
Pantanal of Poconé Region (Mato Grosso, Brasil). Water Air Soil Pollut. 125 (1),
M., Tilvi, S., Singh, K., 2019. Molecular characteristics of sedimentary organic
319–330.
matter in controlling mercury (Hg) and elemental mercury (Hg0) distribution in
Cardoso, P.G., Sousa, E., Matos, P., Henriques, B., Pereira, E., Duarte, A.C., Pardal, M.A.,
tropical estuarine sediments. Sci. Total Environ. 668, 592–601.
2013. Impact of mercury contamination on the population dynamics of Peringia
Prokop, Z., Cupr, P., Zlevorova-Zlamalikova, V., Komarek, J., Dusek, L., Holoubek, I.,
ulvae (Gastropoda): implications on metal transfer through the trophic web.
2003. Mobility, bioavailability, and toxic effects of cadmium in soil samples.
Estuar. Coast. Shelf Sci. 129, 189–197.
Environ. Res. 91 (2), 119–126.
Chakraborty, P., 2017. Mercury exposure and Alzheimer’s disease in India-An
Ramaswamy, V., Rao, P.S., 2006. Grain size analysis of sediments from the Northern
imminent threat? Sci. Total Environ. 589, 232–235.
Andaman Sea: comparison of laser diffraction and sieve-pipette techniques. J.
Chakraborty, P., Babu, P.R., Acharyya, T., Bandyopadhyay, D., 2010. Stress and
Coast. Res. 224, 1000–1009.
toxicity of biologically important transition metals (Co, Ni, Cu and Zn) on
Rauret, G., Lopez-Sanchez, J.F., Sahuquillo, A., Rubio, R., Davidson, C., Ure, A.,
phytoplankton in a tropical freshwater system: An investigation with pigment
Quevauviller, P., 1999. Improvement of the BCR three step sequential extraction
analysis by HPLC. Chemosphere 80 (5), 548–553.
 K. Chennuri et al. / Science of the Total Environment 701 (2020) 134842 9

procedure prior to the certification of new sediment and soil reference standard absorption bands in holmium oxide solution for UV/visible molecular
materials. J. Environ. Monit. 1 (1), 57–61. absorption spectrophotometry. J. Phys. Chem. Ref. Data 34 (1), 41–56.
Ravichandran, M., 2004. Interactions between mercury and dissolved organic Noaa, U., 1999. Sediment Quality Guidelines Developed for the National Status and
matter––a review. Chemosphere 55 (3), 319–331. Trends Program.
Reid, D.G., Ozawa, T., 2016. The genus Pirenella Gray, 1847 (= Cerithideopsilla Van Leeuwen, H.P., Town, R.M., Buffle, J., Cleven, R.F., Davison, W., Puy, J.,
Thiele, 1929)(Gastropoda: Potamididae) in the Indo-West Pacific region and van Riemsdijk, W.H., Sigg, L., 2005. Dynamic speciation analysis and
Mediterranean Sea. Zootaxa 4076 (1), 1–91. bioavailability of metals in aquatic systems. Environ. Sci. Technol. 39 (22),
Renneberg, A.J., Dudas, M.J., 2001. Transformations of elemental mercury to 8545–8556.
inorganic and organic forms in mercury and hydrocarbon co-contaminated Vazquez, M.J., Carro, A.M., Lorenzo, R.A., Cela, R., 1997. Optimization of
soils. Chemosphere 45 (6–7), 1103–1109. methylmercury microwave-assisted extraction from aquatic sediments. Anal.
Rooney, J.P., 2007. The role of thiols, dithiols, nutritional factors and interacting Chem. 69 (2), 221–225.
ligands in the toxicology of mercury. Toxicology 234 (3), 145–156. Vudamala, K., Chakraborty, P., Sailaja, B.B., 2017. An insight into mercury reduction
Rytuba, J.J., 2000. Mercury mine drainage and processes that control its process by humic substances in aqueous medium under dark condition.
environmental impact. Sci. Total Environ. 260 (1–3), 57–71. Environ. Sci. Pollut. Res. 24 (16), 14499–14507. https://doi.org/10.1007/
Sarkar, S.K., Bhattacharya, B., Bandopadhaya, G., Giri, S., Debnath, S., 1999. Tropical s11356-017-8979-4.
coastal organisms as qualitative indicators of mercury and organomercury for Wallschläger, D., Desai, M.V., Wilken, R.D., 1996. The role of humic substances in the
sustainable use of living resources. Environ. Dev. Sustain. 1 (2), 135–147. aqueous mobilization of mercury from contaminated floodplain soils. Water Air
Schartup, A.T., Ndu, U., Balcom, P.H., Mason, R.P., Sunderland, E.M., 2015. Soil Pollut. 90 (3–4), 507–520.
Contrasting effects of marine and terrestrially derived dissolved organic Wang, W.X., Stupakoff, I., Gagnon, C., Fisher, N.S., 1998. Bioavailability of inorganic
matter on mercury speciation and bioavailability in seawater. Environ. Sci. and methylmercury to a marine deposit-feeding polychaete. Environ. Sci.
Technol. 49 (10), 5965–5972. Technol. 32 (17), 2564–2571.
Taylor, D.L., Linehan, J.C., Murray, D.W., Prell, W.L., 2012. Indicators of sediment and Yu, X., Li, H., Pan, K., Yan, Y., Wang, W.X., 2012. Mercury distribution, speciation and
biotic mercury contamination in a southern New England estuary. Mar. Pollut. bioavailability in sediments from the Pearl River Estuary, Southern China. Mar.
Bull. 64 (4), 807–819. Pollut. Bull. 64 (8), 1699–1704.
Travis, J.C., Acosta, J.C., Andor, G., Bastie, J., Blattner, P., Chunnilall, C.J., Crosson, S.C., Zvonareva, S., Kantor, Y., 2016. Checklist of gastropod molluscs in mangroves of
Duewer, D.L., Early, E.A., Hengstberger, F., Kim, C.S., 2005. Intrinsic wavelength Khanh Hoa province, Vietnam. Zootaxa 4162 (3), 401–437.