Dynamics of mercury content in adult sichel (Pelecus cultratus L.) tissues from the Baltic Sea before and during spawning

Marine Environmental Research 148 (2019) 75–80

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Dynamics of mercury content in adult sichel (Pelecus cultratus L.) tissues from the Baltic Sea before and during spawning

T

Joanna Nowosada, Justyna Sieszputowskaa, Dariusz Kucharczyka,∗, Joanna Łuczyńskab, Mateusz Sikoraa, Roman Kujawaa a b

Department of Lake and River Fisheries, University of Warmia and Mazury, Olsztyn, Poland Department of Commodity Science and Food Analysis, University of Warmia and Mazury, Olsztyn, Poland

A R T I C LE I N FO

A B S T R A C T

Keywords: Baltic sea Heavy metals Mercury Muscles Ovaries Pollutions

This study compares the content of mercury in the muscles, liver, kidneys, gonads and gills of male and female individuals of sichel (Pelecus cultratus). Moreover, the trend of changes of mercury concentration before (March) and during (May) the spawning season was examined. Sichel brooders were caught in the Vistula Lagoon during commercial fishing. The mercury content in tissues was determined by atomic absorption using a Milestone DMA-80. The tests revealed a statistically higher mercury concentration in muscles, liver and gonads in male vs. female fish. Moreover, significantly higher mercury concentration was found in male and female fish caught during the spawning season (May) than in those caught before this season (March). Moreover, testes (0.011 ± 0.007 mg kg−1 w/w) were found to contain 12 times, and ovaries (0.004 ± 0.001 mg kg−1 w/w) – approx. 19 times less mercury than the muscular tissue of those same fish. This may suggest the existence of a protective barrier, defending future offspring against the transfer of toxic mercury from the parent body to gonads and gametes.

1. Introduction The development of civilisation and technology has led to a significant upsetting of the homeostasis of the natural environment, among other things, as a result of the natural environment pollution, mainly of aquatic biocenoses. For decades, liquid waste of various origins has been discharged to the environment; it often contains organic compounds harmful to living organisms, including heavy metals. This results in their considerable accumulation in the environment. Pollution of water has a negative effect on the condition of the entire environment, organisms living in them and - indirectly - on humans (Nwabunike, 2016). Pollution of aquatic ecosystems may result in high mortality of living organisms and bring about adverse changes in their behaviour, growth and reproduction (Drevnick and Sandheinrich, 2003). Aquatic organisms developing in improper environmental conditions can have impaired immunity and may be susceptible to various parasitic, contagious diseases and cancers (Jezierska et al., 2009; Jiang et al., 2018). However, the increasing concentrations of heavy metals are the worst type of pollution, including heavy metals originating from industrial gases, precipitates, sewage, particulates, combustion of coal and other

∗

fuels (Morel et al., 1998; Falandysz et al., 2000). It is noteworthy that this hazard arises from the permanent nature of the contamination, resulting - among other things - from an inability to decompose heavy metals. Chemical compounds in the environment can be dissolved or undissolved, situated in water, deposits and in tissues of living organisms (Brown and Austin, 2012; Łuczyńska et al., 2017). Heavy metals, such as cadmium (Cd), mercury (Hg), lead (Pb), arsenic (As) can cause serious damage to the body. These elements can be transported into the body through the respiratory system (e.g. gills), the alimentary tract, adsorption through the body cover or by consumption of other contaminated organisms in the trophic chain (Govind and Madhuri, 2014; Nwabunike, 2016). After taking up such metals, an organism can absorb, accumulate (bioaccumulation), transform or eliminate them to a small extent. If the regulation of the concentration of heavy metals in animal organisms decreases, bioaccumulation in differences tissues takes place (Barwick and Maher, 2003). The level of accumulation of heavy metals in the animals body is affected by the fish size, their age, type of food consumed and the contamination level of aquatic biocenoses inhabited by them (Esteve et al., 2012; Nwabunike, 2016). Mercury (Hg) is one of the most hazardous environmental

Corresponding author. E-mail address: [email protected] (D. Kucharczyk).

https://doi.org/10.1016/j.marenvres.2019.05.010 Received 19 November 2018; Received in revised form 11 May 2019; Accepted 13 May 2019 Available online 14 May 2019 0141-1136/ © 2019 Elsevier Ltd. All rights reserved.

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Table 1 Characteristics of sichel Pelecus cultratus spawners: males (M) and females (F), before (M – BS, n = 14; F–BS; n = 14), during (M – DS, n = 14; F – DS., n = 14) and after spawning (F – AS, n = 4) used in presented study. Males and females were compared separately. Data (mean ± SD) in rows marked with different letters were statistically different (P < 0.05). Parameters

Group M–BS

Mean body weight [g] Mean body length [cm] GSI [%]

216.6 ± 32.6 34.3 ± 1.9 1.1 ± 0.3a

M–DS

F–BS

228.7 ± 41.1 34.8 ± 1.5 0.8 ± 0.1b

F – AS

F–DS

246.5 ± 26.5 35.6 ± 1.2 6.9 ± 1.6B

B

318.0 ± 64.5 36.7 ± 2.2 14.9 ± 3.3A

A

236.8 ± 23.5B 35.9 ± 0.9 1.5 ± 0.4C

2. Material and methods

pollutants. It occurs in various physical and chemical forms, it has unique toxicity towards all organisms (Lesniewska et al., 2009). The major mercury species include elemental mercury, inorganic mercury, methylmercury and dimethylmercury (EFSA, 2012; Govind and Madhuri, 2014). They have different properties, ultimate distribution in the body, level of toxicity, mobility in the environment, potential for bioaccumulation and biomagnification in the trophic chain (Barwick and Maher, 2003; Brown and Austin, 2012; Polak-Juszczak, 2017). Exposure of organisms, such as fish, to the toxic effects of mercury, contributes to contamination of entire trophic systems. Negative outcomes of accumulation of this heavy metal include reproduction disturbance (Drevnick and Sandheinrich, 2003), neurological disorders (Gilbert and Grant-Webster, 1995; Castoldi et al., 2001) and sensory damage (Tanan et al., 2006). Methylmercury affects gonad development, it can impair reproductive success by a decrease in the percentage of larvae hatching and their survival rate (Baillon et al., 2015). Studies of mercury content in fish tissues can reflect the extent of pollution of the environment inhabited by them (Fatima et al., 2014; Baillon et al., 2015; Nwabunike, 2016). The most important reactions which produce mercury species easily absorbed by organisms include a change of the degree of oxidation and formation of methylmercury compounds (Wolfe et al., 1998). Contamination of marine organisms with methylmercury compounds has its source mainly in algae and bacteria (Atwell et al., 1998; Campbell et al., 2005). Subsequently, the contamination is transferred to higher order consumers according to the food chain direction, with humans at the end of it (EFSA, 2004; Brown and Austin, 2012). Sichel Pelecus cultratus is a rheophilic fish of the cyprinid family (Cyprinidea), the only representative of the genus Pelecus (Kujawa et al., 2017). Fish of this species inhabit water with low salinity of 0.3–5.0‰, freshwater rivers and artificial reservoirs in large area of Eurasia. Sichel is a semi-migrating and sedentary fish. During the reproductive period, sichel migrates to fresh waters, usually to rivers flowing to the sea or to coastal bays, in order to lay a one-portion spawn (Kujawa et al., 2017). Eggs of the sichel are pelagic, which is why spawn occurs at a depth of 1.5–7 m to prevent them from falling to the bottom (Kujawa and Mamcarz, 2014). In Poland, sichel is regarded as a rare and endangered species (Krzykawski and Więcaszek, 1997) and it is on the Polish list of fish and lampreys as a critically threatened (CR) species (Witkowski et al., 2009). It is also mentioned in Appendix III of the Bern Convention (protected fauna species). The status of the species has necessitated starting work on the biotechnology of reproduction and the production of stocking material of the species in controlled conditions (Kujawa et al., 2016, 2017) in order to protect the species actively. Sichel has been the object of studies in which mercury content in muscles was determined (Falandysz et al., 2000; Zarei et al., 2011), but no assays of mercury in other tissues (organs) have been conducted nor have the trends in the change of metal content been compared in males and females before and during the reproductive period. The aim of the study was to determine the content of mercury in tissues (in gills, liver, kidney, muscles, gonads) of the sichel Pelecus cultratus caught in waters of the Vistula Lagoon before and during the spawning season of the species.

2.1. Fish sampling Brooders of the sichel were caught in the waters of the Vistula Lagoon (a bay of the Baltic Sea) with a herring net, 8 km from Frombork towards Piaski (March; 54°41ꞌN, 19°60ꞌE) and with fyke nets approximately 1 km from Frombork towards Nowa Karczma (May; 54°36ꞌN’, 19°67ꞌE) during commercial fishing. Samples for tests (n = 60) were caught at two dates: two months before the spawning season (22 March 2017; n = 28) – BS (before spawning) group, and during the spawning season (22 May 2017; n = 32) – DS (during spawning) group. Brooders were transported to the Centre for Aquaculture and Ecological Engineering, where they were weighed ( ± 0.01 g), measured ( ± 0.1 mm) and had their tissue samples (liver, gills, kidney, muscles and gonads) collected in order to determine the total mercury content in them. During the tissue sampling, the fish sex was determined and samples were taken separately for males – M group – and females – F group. Additionally, the gonads (ovaries and testes) were weighed ( ± 0.01 g) and the gonadosomatic index (GSI) was calculated. Samples from 14 individuals were taken in each group. Additionally, 4 spawned females were found among the fish caught in May, of which tissue samples were also taken – F-AS group (after spawning) (Table 1). The sample tissues were stored in an ultra-low temperature freezer (Sanyo, MDF-U32V) at −80 °C until analysis. The gonadosomatic index was calculated from the formula: GSI = (GW BW−1) 100%, where GW: gonad weight (g), BW: body weight (g). 2.2. Determination of mercury Duplicate samples of up to 0.05 g ( ± 0.0001 g) of fish tissues (muscle, gonads, kidney, liver, gills) were weighed and analysed as total mercury measured by atomic absorption thermal decomposition using a Milestone DMA-80 (with dual cell). The first step involved drying at 200 °C (for samples, including fish, with high water content). The purging time (the time between the end of drying/decomposition and the start of Hg measurement) was 60 s. The amalgam heater time (the time necessary for mercury release and its collection into an absorption cuvette) was 12 s. The signal recording time was 30 s. The parameters for drying and decomposition (temperature/time, respectively) were as follows: max. start temp. 200 °C 60 s−1, drying temperature 160 °C 60 s−1; decomposition (burned in an oxygen flow) at 650 °C 60 s−1. The time between the termination of drying and the onset of decomposition (650 °C) was 120 s. The absorption wavelength was 253.65 nm (at a detection limit of 0.005 ng Hg) and the detector consisted of UV enhanced photodiodes. The analysis method was tested by measuring the elements in reference material: BCR CRM 422 (muscles of Atlantic cod Gadus morhua (L.)). The certified content of Hg was 0.559 ± 0.016 mg kg−1 The percentage recovery rate was 100.2% (n = 4). 2.3. Data analysis Data 76

were

presented

as

mean

with

standard

deviation

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Fig. 1. Relationship between concentration of mercury (mg kg−1 wet weight) in muscles depending on body weight of males (A; n = 28) and females (B; n = 32) of sichel, Pelecus cultratus. Data expressed as the mean ± SD.

and in females (n = 32) of the sichel was found in muscles (0.139 ± 0.036 and 0.116 ± 0.033 mg kg−1 wet weight, for males and females, respectively). The significantly lowest (P < 0.05) concentration of mercury was found in gills (0.016 ± 0.005 and 0.016 ± 0.006 mg kg−1 w/w in males and females) and in gonads (0.011 ± 0.007 and 0.006 ± 0.003 mg kg−1 in males and females, respectively). Moreover, testes were found to contain 12.3 times (0.011 ± 0.007 mg kg−1 wet weight (w/w)), and ovaries – 18.9 times (0.004 ± 0.001 mg kg−1 w/w) less mercury than the muscular tissue of both sexes (P < 0.05; Fig. 2). Moreover, significant differences were found (P < 0.05) in mercury concentration in tissues of fish obtained before (March) and during (May) the spawning season (Fig. 3). A significant increase (P < 0.05) in mercury content in muscles (0.117 ± 0.027 to 0.164 ± 0.028 mg kg−1 w/w), kidney (0.033 ± 0.009 to 0.080 ± 0.015 mg kg−1 w/w), liver (0.037 ± 0.011 to 0.072 ± 0.018 mg kg−1 w/w) and in testes (0.005 ± 0.001 to 0.018 ± 0.004 mg kg−1 w/w) was found in males during the spawning season (group M – DS; n = 14), compared to males caught before the spawning season (group M – BS; n = 14). The analysis of the sichel female gonads after the spawning season (GSI = 1.5 ± 0.4%; 0.012 ± 0.002 mg kg−1 w/w), which found a considerable concentration of mercury (P < 0.05) compared to gonads in females which did not start the spawn (GSI = 14.9 ± 3.3%; 0.007 ± 0.002 mg kg−1 w/w), may indicate that only a small amount of mercury has been eliminated from the mother's body with eggs (Fig. 4). A significant correlation (R 2 = 0.614; P = 0.00) was also observed between GSI (gonadosomatic index) and mercury concentration in testes (Fig. 4a). A significantly (P < 0.05) lower mercury content was found in all tissues in females before the reproductive period (group F–BS; n = 14) than in females during the reproductive period (group F – DS; n = 14; Fig. 3b). Moreover, a significantly higher mercury content was found in ovaries of females after the spawning season (group F – AS; 0.012 ± 0.002 mg kg−1 w/w; n = 4) (which resulted in a statistically lower (P < 0.05) GSI) compared to the females from before spawn (group F–BS; 0.004 ± 0.001 mg kg−1 w/w; n = 14) and during the spawning season (group F – DS; 0.007 ± 0.002 mg kg−1 w/ w; n = 14) (Fig. 3b).

(mean ± SD). Percentage data were subjected to arcsin transformation before they were analysed statistically. The mercury concentrations, body weight, body length, GSI were tested for normality (Shapiro-Wilk test) and homogeneity of variance (test Levene's). Statistically significant differences (α = 0.05) were determined using one-way analysis of variance (ANOVA), followed by parametric (t-test or Tukey's) or nonparametric (Mann–Whitney U test or Kruskal-Wallis) post-hoc tests. Relationships between concentrations in the tissues and organs of fish (non-parametric data) were tested using Microsoft Excel and Spearman's rank correlation test. The statistical analysis was conducted with Microsoft Excel and Statistica v. 13.1 (StatSoft Inc., USA).

3. Results The study revealed a significant correlation between the brooders’ weight and mercury content in muscles, both in females (n = 32; R2 = 0.506; P = 0.00) and in males (n = 28; R2 = 0.701; P = 0.00) (Fig. 1). It has also been shown that mercury accumulates in individual tissues in similar proportions in females (n = 32; total groups: F–BS, F – DS and F – AS) and in males (n = 28; total groups: M – BS, M – DS) of the sichel (Fig. 2). However, it was found that the content of mercury in females was significantly (P < 0.05) lower in muscles (1.2 times), liver (1.3 times) and gonads (1.8 times) compared to males (Fig. 2). The highest concentration of mercury (P < 0.05), both in males (n = 28)

Mercury content [mg kg-1]

0.2

a

male

0.16

female

b

0.12

a

0.08

a

a b

0.04 0

a a

*

muscle

**

kidney

**

liver

***

gills

a

b

***

4. Discussion

gonads

Fig. 2. Concentration of mercury (mg kg−1 wet weight) in males (n = 28) and females (n = 32) tissues: muscle, kidney, liver, gills and gonads. Data (mean ± SD) in bars marked with different letters were statistically different in separate tissue (P < 0.05). Data marked with different number of asteroids (*) are different between mercury concentration in tissue (P < 0.05).

Mercury is a highly toxic element, which occurs in the environment as various species (Park and Zheng, 2012). Methylmercury is regarded as the most toxic mercury form, which is intensively accumulated in aquatic fauna and flora. It is assumed hypothetically that predators, which are at the top of the food pyramid, contain more mercury than 77

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Fig. 3. Concentration of mercury (mg kg−1 wet weight) in males - M (A) and females - F (B) tissues: muscle, kidney, liver, gills and gonads, before (M – BS, n = 14; F–BS; n = 14), during (M – DS, n = 14; F – DS., n = 14) and after spawning (F – AS, n = 4). Data (mean ± SD) in bars marked with different letters were statistically different in separate tissue (P < 0.05).

TL = 34.3–36.7 cm; W = 216.6–318.0 cm), where up to 2.08 ± 1.19 mg kg−1 was found in muscles (Subotic et al., 2015), and in the Caspian Sea in Iran – 0.17 ± 0.11 mg kg−1 wet weight (Zarei et al., 2011). This may suggest that the Danube River is more polluted with mercury than the Caspian Sea and the Vistula Lagoon, which is part of the Baltic Sea, because smaller fish from Danube river accumulated higher amount of mercury than larger sichel from other geographic locations. Interestingly, this study has shown that male sichel have significantly more mercury accumulated in muscles, liver and gonads than females (Fig. 2). Similar situation was noted e.g. in flounder and great cormorant (Phalacrocorax carbo) (Napierska and Podolska, 2008; Misztal-Szkudlińska et al., 2011; Polak-Juszczak, 2012). In many fish species and in sichel males at the same age as females are smaller and lighter. So, if they eat similar amount of food, the same amount of mercury accumulate in smaller weight, what in consequence, means the higher mercury concentration in the tissues. What is it interesting, the, higher concentrations of mercury in the tissues under study were found in the sichel caught during the spawning season compared to the fish caught two months earlier (Fig. 3). There is a few possibilities of such situation. This may be attributed to the fact that the migrating form of the sichel swim to the spawning ground closer to the coast, which is usually more polluted than open waters (Polak-Jaszczuk, 2012). Immediately before the spawn, brooders need a lot of nutrients to build gonads, which is why they feed in the littoral zone. Also, it might be an effect of the extraction of protein reserves from muscle resulting in higher concentrations of Hg in a smaller amount of tissue. It also might

the species from lower levels of the trophic chain (Misztal-Szkudlińska et al., 2018). Mercury found in tissues of sichel probably got there through the trophic chain and by taking up this heavy metal from water through the gills (Hall et al., 1997). Being a heavy metal, mercury accumulates in plankton and phytoplankton (Mason et al., 1995; Atwell et al., 1998; Campbell et al., 2005), on which planktivorous, such as sichel, feed. Present study has revealed a significant correlation between mercury content in muscles and the weight of sichel brooders (P < 0.05); the highest amounts were found in the largest fish (Fig. 4). Similar situation has also been observed in other fish species, e.g. Atlantic cod (Gadus morhua), European eel (Anguilla anguilla), European perch (Perca fluviatilis), herring (Clupea harengus), flatfish (Platichthys flesus) (Polak-Juszczak and Robak, 2015; Polak-Juszczak, 2012, 2017; Nowosad et al., 2018). It suggest that in sichel, as well as in other fish species, mercury accumulate whole live, and larger (probably also older) fish had higher level of mercury in their tissue. Such phenomenon might be negative results on reproduction of oldest fish in populations due to the highest level of mercury. This study has shown that the mercury concentration in these tissues was significantly lower compared to its content in muscles (P < 0.05), similarly, as stated by the authors of other fish species (Polak-Juszczak, 2012; Nowosad et al., 2018). It was found in this study for the sichel from the Baltic Sea river basin that the mercury concentration is lower (0.127 ± 0.037 mg kg−1 w/w; n = 64; Table 1) in its muscles compared with sichel caught in the Danube River in Serbia (TL = 28.77 ± 4.28 cm; W = 142.00 ± 68.14 g vs. in present study (mean ranges)

Fig. 4. Relationship between concentration of mercury (mg kg−1 wet weight) in testis (A; n = 28) and ovary (B; n = 28) depending on gonadosomatic index (GSI) sichel, Pelecus cultratus. Data expressed as the mean ± SD. 78

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be linked with high metabolism during final gamete maturation. The differences in mercury level in fish tissue in different year seasons was noted for of perch (Perca fluviatilis) by Szefera et al., 2003). It suggest that the heavy metals content in fish tissue not only increased by year to year but also was dynamic during different seasons. Pollution in the fish body can inhibit gonad growth and delay and weaken their maturation (Dietrich et al., 2010; Baillon et al., 2015). Drevnick and Sandheinrich (2003) demonstrated that exposing sexually mature fish to low concentrations of mercury does not affect their growth and survival rate, but it impairs the reproductive success. Aquatic organisms exposed to higher concentrations of this heavy metal delayed the spawn (Hammerschmidt et al., 2002). Mercury can decrease the level of testosterone in plasma in males and 17-β-oestradiol in females. This resulted in inhibition of ovary development and in decreasing the percentage of ovulation (Drevnick and Sandheinrich, 2003) and it has shown that a spawning school exposed to even small amounts of mercury can decrease the success of reproduction, including fertilisation and the survival rate of embryos and larvae following hatching (Dietrich et al., 2010; Bridges et al., 2015). Exposing spawn to the toxic effect of mercury can, in effect, result in premature hatching of larvae (Ismail and Yusof, 2011) as a result of hypoxia, metabolic processes are disturbed along with cellular membranes. Fish larvae hatched from spawn exposed earlier to mercury are susceptible to various developmental anomalies and motor irregularities (Bridges et al., 2015). Exposing fish to toxic substances at early stages of their lives can lead to negative, irreversible effects even at lower concentrations than in adult fish. Early stages of fish development are the most sensitive indicator of many types of water pollution (Devlin and Mottet, 1992; Pickering and Lazorchak, 1995; Devlin, 2006). The level of mercury found in sichel in present study was much lower than found in the species originated from Danube river (Subotic et al., 2015). It might suggested, that mercury concentration in sichel tissue from Baltic Sea were not be harmful. Assuming that a certain amount of mercury accumulated in the body of a parent would reach the embryo, it would mean that the offspring would be condemned to congenital defects or death. However, observations of organisms living in the wild have shown that at least some organisms (e.g. European eel) defend themselves against environmental pollution and species extinction by developing a barrier preventing the transfer of toxic mercury from the mother's body to an egg (of future offspring) (Nowosad et al., 2018). This may be supported by the argument that in sichel (this study), ovaries were found to contain 18.9 and testes - 12.3 times less mercury than muscles of female and male fish, respectively (Fig. 3). A study by Nowosad et al. (2018) showed that the content of mercury in female European eels is 78 times lower in spawn than in muscles, and its content in eggs (0.0031 mg kg−1) is eight times lower than in gonads (0.026 mg kg−1). This indicates that only a small amount of mercury crosses the barrier between the mother's body and eggs (growing embryo). Kwasniak and Falkowska (2012), found eggs to be of little importance in detoxification of mercury in the body of Atlantic cod females from the Baltic Sea. Gonads (0.020 ± 0.014 mg kg−1) of the cod were found to contain 5.4 times less mercury than muscles (0.108 ± 0.099 mg kg−1). In their study, Baillon et al. (2015) proved genes of fish exposed to pollutants protect the organism against oxidative stress, were involved in DNA repair, synthesis of steroid hormones and in oocyte maintenance. On the other hand, a study by Dietrich et al. (2010) suggests the existence of a protective barrier made up of albumins present in semen plasma, which bind with mercury ions, thereby restricting the transfer of the metal to sperm. This would explain, to a certain extent, the findings of present study in which the mercury content in testes was found to be the lowest of all tissues/organs and, on the other hand, an increase in mercury content during the reproductive period, with a simultaneous decrease in the GSI (Table 1). This suggests that sperm were expelled during the spawning practically without mercury, which remained in the testes. It was exactly the same with sichel females. These findings

coincide with those described for female eel (Nowosad et al., 2018), where this metal concentration in the ovaries also increased after spawn (practically mercury-free) was expelled. The mercury level in sichel tissues is relatively low, which may suggest that waters of the Baltic Sea are not strongly contaminated with mercury compounds. The study has shown that the mercury level in tissues varies and is higher during the spawning season. Moreover, males accumulate more mercury in muscles, liver and gonads compared with females. The lowest concentrations were found in gonads of both males and females, which may suggest the existence of a barrier protecting future offspring against the transfer of hazardous mercury from parent bodies. Acknowledgement The study was financed by Warmia and Mazury University in Olsztyn, Poland, grant No. 18.610.005-300. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marenvres.2019.05.010. References Atwell, L., Hobson, K.A., Welch, H.E., 1998. Biomagnification and bioaccumulation of mercury in an arctic marine food web: insights from stable nitrogen isotope analysis. Can. J. Fish. Aquat. Sci. 55, 1114–1121. Baillon, L., Oses, J., Pierron, F., Bureau du Colombier, S., Caron, A., Normandeau, E., Lambert, P., Couture, P., Labadie, P., Budzinski, H., 2015. Gonadal transcriptome analysis of wild contaminated female European eels during artificial gonad maturation. Chemosphere 139, 303–309. Barwick, M., Maher, W., 2003. Biotransference and biomagnifications of selenium, cadmium, zinc, arsenic and lead in a temperate seagrass ecosystem from Lake Macquarie Estuary, NSW, Australia. Mar. Environ. Res. 56, 471–502. Bridges, K.N., Soulen, B.K., Overturf, C.L., Drevnick, P.E., Roberts, A.P., 2015. Embryotoxicity of maternally transferred methylmercury to fathead minnows (Pimephales promelas). Environ. Toxicol. Chem. 35 (6), 1436–1441. Brown, I.A., Austin, D.W., 2012. Maternal transfer of mercury to the developing embryo/ fetus: is there a safe level? Toxicol. Environ. Chem. 94 (8), 1610–1627. Campbell, L., Norstrom, R., Hobson, K., Muir, D., Backus, S., Fisk, A., 2005. Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay). Sci. Total Environ. 351–352, 247–263. Castoldi, A.F., Coccini, T., Ceccatelli, S., Manzo, L., 2001. Neurotoxicity and molecular effects of methylmercury. Brain Res. Bull. 55, 197–203. Devlin, E.W., 2006. Acute toxicity, uptake and histopathology of aqueous methyl mercury to fathead minnow embryos. Ecotoxicology 15 (1), 97–110. Devlin, E.W., Mottet, N.K., 1992. Embryotoxic action of methylmercury on coho salmon embryos. Bull. Environ. Contam. Toxicol. 49, 449–454. Dietrich, G.J., Dietrich, M., Kowalski, R.K., Dobosz, S., Karol, H., Demianowicz, W., Glogowski, J., 2010. Exposure of rainbow trout milt to mercury and cadmium alters sperm motility parameters and reproductive success. Aquat. Toxicol. 97 (4), 277–284. Drevnick, P.E., Sandheinrich, M.B., 2003. Effects of dietary methylmercury on reproductive endocrinology of fathead minnows. Environ. Sci. Technol. 37 (19), 4390–4396. EFSA (European Food Safety Authority Scientific), 2004. Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to mercury and methylmercury in food. EFSA J 34, 1–14. EFSA (European Food Safety Authority Scientific), 2012. Opinion on the risk for public health related to the presence of mercury and methylmercury in food. EFSA J 10 (12), 2985. Esteve, C., Alcaide, E., Urena, R., 2012. The effect of metals on condition and pathologies of European eel (Anguilla anguilla): in situ and laboratory experiments. Aquat. Toxicol. 109, 176–184. Falandysz, J., Chwir, A., Wyrzykowska, B., 2000. Total mercury contamination of some fish species in the firth of Vistula and the lower Vistula river, Poland. Pol. J. Environ. Stud. 9 (4), 335–339. Fatima, M., Usmani, N., Hossain, M.M., 2014. Heavy metal in aquatic ecosystem emphasizing its effect on tissue bioaccumulation and histopathology: a review. J. Environ. Sci. Technol. 7 (1), 1–16. Gilbert, S.G., Grant-Webster, K.S., 1995. Neurobehavioural effects of developmental methylmercury exposure. Environ. Health Perspect. 103 (6), 135. Govind, P., Madhuri, S., 2014. Heavy metals causing toxicity in animals and fishes. Res. J. Anim., Vet. Fish. Sci. 2 (2), 17–23. Hall, B.D., Bodaly, R.A., Fudge, R.J.P., Rudd, J.W.M., Rosenberg, D.M., 1997. Food as the dominant pathway of methylmercury uptake by fish. Water, Air, Soil Pollut. 100 (1–2), 13–24.

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