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Open AccessFeature PaperArticle

Environmental Investigations and Tissue Bioaccumulation of Heavy Metals in Grey Mullet from the Black Sea (Bulgaria) and the Ionian Sea (Italy)

1
Department of Veterinary Sciences, Polo Universitario Annunziata, University of Messina, 98168 Messina, Italy
2
Institute for Marine Biological Resources and Biotechnology (IRBIM), National Research Council (CNR), Section of Messina, Spianata S. Raineri 86, 98122 Messina, Italy
3
Department of Chemistry, Faculty of Pharmacy, Medical University Varna, 84 Tzar Osvoboditel Blv, 9000 Varna, Bulgaria
*
Author to whom correspondence should be addressed.
Animals 2020, 10(10), 1739; https://doi.org/10.3390/ani10101739
Received: 11 September 2020 / Accepted: 21 September 2020 / Published: 24 September 2020
(This article belongs to the Special Issue Diseases in Laboratory and Wild Aquatic Organisms)
The environmental monitoring of dangerous chemicals and how these affect the aquatic biota is of fundamental importance in defining the health status of fish. Pollution with chemical elements is of great environmental concern, since fish and marine organisms can uptake various toxicants and subsequently transfer them to man through the food web. Moreover, the accumulation of toxic elements could be a cause of pathology insurgence in fish. These organisms represent a good indicator of the status of coastal water. Flathead grey mullet (Mugil cephalus) is a coastal species, bottom dwelling and feeding on detritus, invertebrates, and algae. The main aim of the present study was to determine the total concentration of nine elements (Cd, Cr, Pb, Ni, Al, Cu, Fe, Mn, and Zn) in the fish species M. cephalus and in coastal marine waters collected from various sampling points along the Black Sea (Bulgaria) and the Ionian Sea (Italy) and to apply those results to the prediction of the pollution status of those coastal marine environments. To achieve this goal, metal concentrations were analyzed in various fish tissues (gills, liver, and muscle) of grey mullet (M. cephalus) and in marine water samples collected from the sampling stations across both areas (Ionian Sea (Italy) and Black Sea (Bulgaria)). The results revealed significant differences within the tissues examined and the marine water samples, principally attributable to the pollution of the area, the bioavailability of metals, and the hydrological conditions. The present study represents the first attempt to compare the data obtained from analyzing sampling points in order to define the different elemental concentrations in M. cephalus muscle tissue and how they reflect environmental ones.

Abstract

The environmental monitoring of chemical toxicants has been a widely studied topic in the last few decades. The main aim of the present study was to determine the total concentration of nine elements (Cd, Cr, Pb, Ni, Al, Cu, Fe, Mn, and Zn) in the fish species grey mullet (M. cephalus) and in the coastal marine waters collected from various sampling points along the Black Sea (Bulgaria) and the Ionian Sea (Italy). Further, those results were applied to predict the pollution degree in those coastal marine environments. The fish samples were subject to acid digestion followed by appropriate analytical determination. The metal concentrations in marine water samples collected from the Black Sea (Bulgaria) and the Ionian Sea (Italy) were also analyzed. Unpaired Student’s t-test and the one-way ANOVA were applied for the statistical analysis of the data. The statistical results revealed a significant variation (p < 0.0001) in the concentration of various fish tissues. The accumulation of toxic and essential elements differs significantly in grey mullet species caught from the Black Sea (Bulgaria) and the Ionian Sea (Italy). The results from this study may serve as a convenient approach during marine pollution programs set by both countries (Italy and Bulgaria).
Keywords: environmental investigation; Black Sea; Ionian Sea; Mugil cephalus; heavy metals environmental investigation; Black Sea; Ionian Sea; Mugil cephalus; heavy metals

1. Introduction

Pollution with heavy metals is of great environmental concern, since fish and other aquatic organisms can accumulate various toxicants and subsequently transfer them to man through the food web. These organisms represent a good indicator of the status of coastal water [1,2,3,4,5].
Heavy metal uptake is strictly related to the species considered. It depends on the sex, age, size, reproductive cycle, swimming pattern, feeding behavior, hydrological conditions, and geographical location of the fish species [6,7].
Using various marine organisms such as fish for a biomonitoring purpose has many advantages, since these organisms are able to accumulate only the biologically available forms of the heavy metals dissolved in the aquatic environment. Moreover, fish enable the continuous monitoring of the aquatic medium due to their characteristic of uptaking contaminants, also in cases where trace pollutants are near to the detection limits [2].
Heavy metals can be classified as potentially toxic (arsenic, cadmium, lead, mercury, nickel, etc.), probably essential (vanadium, cobalt), and essential (copper, zinc, iron, manganese, selenium) [8]. Toxic elements can be very harmful even at low concentrations when ingested over a long time, and may affects the life cycle stages of fish [9,10]. Additionally, it has been demonstrated that various toxic elements are linked with skeletal deformities in natural fish populations as well as in laboratory-produced ones [11], alterations in lateral lines [12], and effects on hematological and biochemical parameters [13,14]. Essential metals, on the other hand, can also produce toxic effects when the metal intake is excessively elevated [15,16].
The behavior and ecological characteristics of the grey mullet (Mugil cephalus) species makes it suitable for the monitoring of marine coastal metal pollution [17,18,19]. Grey mullet is a bottom-dwelling species that feeds on detritus, microscopic invertebrates, and algae [2,20], and it is known to accumulate a high level of heavy metals in its organs from the surrounding environment [21].
The Black Sea is known to be the largest natural anoxic water basin (below 180 m in depth) in the world. It has very few seawater exchanges with the Mediterranean Sea. However, the Black Sea receives several freshwater inputs from some of Europe’s largest rivers (the Danube, Dniester, and Dnieper) [22]. This, jointly with numerous human activities in the area, has led to it having a highly polluted condition.
The Ionian Sea forms the westernmost part of the eastern Mediterranean basin. The profile of the Ionian Sea has been described by several studies [23,24]. Continuous water exchange and renovation allow a rapid dispersion of contaminants.
The concentrations of heavy metals in fish have been extensively studied over the past several decades, but still there is a lack of information in the scientific literature concerning the heavy metal distribution in the grey mullet species. The aim of the present study was to determine the total concentration of nine heavy elements (Cd, Cr, Pb, Ni, Al, Cu, Fe, Mn, and Zn) in the fish species M. cephalus and in coastal marine waters collected from various sampling points along the Black Sea (Bulgaria) and the Ionian Sea (Italy). Further, we aimed to apply those results to the prediction of the pollution status in those coastal marine environments. To achieve this goal, the metal concentrations were analyzed in various fish tissues (gills, liver, and muscle) of grey mullet (M. cephalus) and in marine water samples collected from the sampling stations across both areas (Ionian Sea (Italy) and Black Sea (Bulgaria)).

2. Materials and Methods

2.1. Fish Sampling

The specimens were caught by bottom-set nets during April 2019. The sampling stations are shown in Figure 1. The sampling stations were selected based on their degree of pollution. The three sampling points across the Ionian Sea were located in an area falling into the Messina Strait boundaries. This area is widely described in the literature [23,25,26,27,28], and it is characterized by strong tidal and stationary currents that continuously mix the Tyrrhenian and Ionian seawater. The sampling points across the Bulgarian Black Sea are recognized as highly populated and industrialized cities.
After capturing, the fish were euthanized using the procedure reported by Iaria et al. [29], modified using 2-phenoxyethanol, and followed by animal welfare procedures with respect to the 2010/63 EU directive [30]. Then, the fish were brought to the laboratory using an icebox, measured with an ichthiometer, and weighted by an electronic balance FX-3000 (max 3100 g precision d = 0.01 g, A & D, 1756 Automation Parkway, San Jose, CA, USA). All the fish were considered healthy based on an external examination for any signs of abnormalities or parasite infestations.

2.2. Sample Preparation, Tissue and Water Analysis

The total lengths and weights of the grey mullet samples brought to the laboratory were measured prior to analysis. The muscles, gills, and liver were dissected and included in representative samples. The samples were weighted, packed in polyethylene bags, and stored at −18 °C until chemical analysis. The biometrics data of the analyzed fish included in this study are shown in Table 1.
Before analysis, the samples were thawed at room temperature and each one was dissected using a stainless steel knife. Each specimen (approximately a portion of 5 g of tissues of interest (muscle, gills, and liver)) was collected and weighed in an analytical balance (precision of 0.1 mg).
The samples of tissue were then subjected to wet digestion, performed in triplicate. Approximately 1.0 g portions of each fish tissue (muscle, liver, and gills) were digested by adding 10 mL of HNO3 (65% Merck, Suprapur, Darmstadt, Germany) in a microwave digestion system MARS 6 (CEM Corporation, Matthews, NC, USA), delivering a maximum power and temperature of 800 W and 200 °C, respectively, and internal temperature control was used to assist the acid digestion process. After complete digestion, the samples were diluted to 25 ml with ultrapure water (resistivity 18 M MΩ; Millipore, Bedford, MA, USA) and stored in pre-cleaned polyethylene bottles until the analysis of the metal concentrations. The blanks were prepared in the same way and were used to calibrate the instrument.
The concentrations of Al, Cd, Cr, Cu, Fe, Mn, Ni, Pb, and Zn in the samples were determined using an ICP-OES Spectrometer (Optima 8000, Perkin Elmer, Waltham, MA, USA) with a plasma gas flow of −10 L/min, an auxiliary gas flow of −0.7 L/min, a nebulizer gas flow of −0.2 L/min, and an axial plasma view. The accuracy of the applied analytical procedure for the determination of heavy metals in fish was tested using DORM-4 (NIST)-certified reference material. Recoveries of between 90.5% and 108% were accepted to validate the calibration.
The marine water samples were collected using polyethylene terephthalate bottles. The collection depth was about 3 m from the surface. The samples were then transferred to the laboratory using a lightproof insulated box containing ice packs.
The heavy metal determination in marine water samples was carried out using atomic absorption spectroscopy (AAS) (Perkin Elmer/AAnalyst 400, Waltham, MA, USA). Different concentrations of standard solutions were carried out to calibrate the AAS for all the metals.

2.3. Statistical Analysis

Prior to statistical analysis, all the data were tested for normal distribution with the Kolmogorov–Smirnov test. All the data were normally distributed and a statistical analysis was performed on the mean values.
AN unpaired Student’s t-test was used to determine significant differences between the metal concentrations (Cd, Cr, Pb, Ni, Al, Cu, Fe, Mn, and Zn) in water samples from the Black Sea versus the Ionian Sea and to compare the metal contents in the water of the two sites.
A one-way analysis of variance (ANOVA) was applied to find significant differences in the metal concentrations of the tissues in grey mullet caught from the Black Sea (Bulgaria) and the Ionian Sea (Italy). Additionally, the ANOVA test was used to assess the differences among metal accumulation in different tissues of grey mullet from the same environment. The level of significance was set at p < 0.05. All the statistical calculations were performed with the statistical software program Prism v. 7.00, 2003 (Graphpad Software Ltd., San Diego, CA, USA).

3. Results

Table 2 shown the heavy metal concentrations (mean ± SD) measured in the seawater of the Black Sea (Bulgaria) and the Ionian Sea (Italy).
The distribution of the different heavy metals along both sampling sites varied considerably, with no clear pattern detected. The most abundant heavy metal in the water samples from the Black Sea was zinc (22.18 μg/L), while that in the Ionian Sea was copper (41.27 μg/L).
Table 3 shows the heavy metal concentrations (mean ± SD) in different M. cephalus tissues for each sampling site in the Black Sea and the Ionian Sea. The heavy metal levels of the grey mullet from the Black Sea (Bulgaria) for all the tissues studied have the following pattern: Fe > Al > Cu > Zn > Mn > Pb > Cr > Ni > Cd. Meanwhile, those from the Ionian Sea (Italy) have the pattern: Fe > Zn> Al > Mn > Cu > Pb > Ni > Cr > Cd. The accumulation patterns of all metals were significantly different (p < 0.001) between the different species, organs, and sites (except for Fe), as well as the different sampling sites (Figure 2 and Figure 3).
All the heavy metals studied (except Zn) exhibited higher concentrations in the analyzed tissues of mullet caught in the Black Sea, Bulgaria, compared to those from the Ionian Sea, Italy.
Additionally, the Black Sea mullet’s liver showed the following maximum concentrations: Cd (0.25 mg/kg w.w), Cu (69.30 mg/kg w.w), Fe (505.75 mg/kg w.w). The gills of the same species caught from the Black Sea had high levels of Cr (0.49 mg/kg w.w), Pb (2.91 mg/kg w.w), Al (52.04 mg/kg w.w), and Mn (31.52 mg/kg w.w). On the contrast, the liver tissues of the grey mullet from the Ionian Sea showed high levels of Ni (0.25 mg/kg w.w) and Zn (34.00 mg/kg w.w). The different levels of heavy metals in the different tissues of the grey mullet is due to the different pattern of tissue accumulation, as shown by various authors [31,32].
In Figure 2, the data of the heavy metals determined and their relative statistical significance for the mullet caught from the Ionian Sea are plotted. The accumulation of heavy metals was predominantly in the liver tissue of M. cephalus for both the Black and Ionian seas. Significant statistical differences resulted for the most of the relations between the heavy metal concentrations in different tissues, except for Cd in the muscle and gills (Figure 2A), Cu in the gills and liver (Figure 2F), and Zn in the muscle and gills (Figure 2I).
Figure 3 shows the graphical elaborations of the heavy metal concentrations in the studied tissues from M. cephalus collected in the Black Sea (Bulgaria). In a few cases, the statistical differences were not significant between the metal concentrations in different tissues, including Ni and Zn in the gills and liver.

4. Discussion

The concentrations of heavy metals detected in the fish of this study were compared with the other reported values in an effort to determine the degree of contamination in the study areas. The reported results in the literature showed that the metal contents in the fish muscles varied widely depending on where the specimens were caught.
As is shown in Figure 2 and Figure 3, the concentration of heavy metals in the muscle tissue is generally lower than that in the gills and liver. These results are in agreement with the ones reported by other authors [33,34,35,36,37]. Dural et al. [38] reported that Cd, Pb, Cu, Zn, and Fe were found with the highest level in muscle tissue in S. aurata, while D. labrax and M. cephalus accumulated the lowest amounts of heavy metals in the muscle.
Heavy metals are absorbed, stored, and detoxified in excess by the fish in the liver [39,40]. Liver is known to be the target organ for the accumulation and detoxification of most metals, independently of the uptake route, representing the optimal tissue for water monitoring. The liver is the organ that maintains for a long time higher concentrations of metals, reflecting proportionally the environmental ones [41].
The gills represent the organ where gas exchange takes place and are involved in the excretion of metal ions, which are excreted in the surrounding water from the body. Furthermore, the mucous excretion of gills has a high binding affinity with metal ions [42]; this and the high metal storage capacity of the gills during their function of absorption and depuration [43,44,45] justified the high concentration of heavy metals found in this tissue.
The higher concentrations of analyzed metals observed in the gills and liver with respect to the muscle are also due to the ability of metallothioneins (proteins synthesized in these organs when fish are exposed to heavy metals) to bind metals and facilitate their detoxification, protecting fish from heavy metal damage [37,45]. The higher heavy metal level in the gills compared to the liver may indicate temporary peaks of the heavy metal concentration in the surrounding waters. Additionally, the high levels of some heavy metals in the liver are related to cases with chronic or long-term heavy metal pollution. Therefore, the low concentrations of metals observed in the muscles would be due to the low levels of binding proteins in these tissues [46].
Moreover, it is widely recognized that muscle tissue does not accumulate most metals, except for mercury, which has a good affinity for this tissue [41,47].
Regarding the metal concentrations in seawater, the present study revealed that significant variations in the metal levels existed in the water of the two sampling regions studied, with a higher concentration of toxic and essential elements in the Ionian Sea with respect to the Black Sea. Despite the fact that the water analyses revealed a higher concentration of most of the studied metals in the Ionian Sea with respect to the Black Sea, this was not confirmed by the grey mullet tissue concentrations. A good explanation of this is that the bioconcentration of contaminants depends on water circulation and renewal. The geographical and hydrological characteristics of the studied environments affects the bioconcentration of such a contaminant. The Black Sea is, in fact, an almost closed basin, with numerous freshwater inputs coming from high-dimension and high-polluted rivers rather than smaller sources in all the Black Sea coastal countries [48]. Once they reach the sea, contaminants in the Black Sea tend to settle in the coastal water, especially because of the scarce water circulation, entering then into food webs, becoming bioavailable, and accumulating in fish species [49]. In contrast, the contaminants in open seas such as the Ionian Sea are continuously dispersed by water circulation and currents. The sampling area of the Ionian Sea is influenced by the high hydrodynamics of Messina’s Strait. Tidal and stationary currents daily renew the coastal water of Messina’s Strait, allowing the dispersion of dissolved metals [26,50,51,52,53]. In addition, the lower concentration of metals in the grey mullet tissues from the Ionian Sea can be due to the low bioavailability of metals in Ionian seawater. It is in fact clear that the bioavailable fractions of metals infer the uptake rates of these contaminants [49]. Pan and Wang [54] demonstrated that direct measurements of metal concentrations in marine environments and food phases cannot provide precise information about metal bioavailability.
The non-significant differences in metals found in seawater from different sampling points in the same area confirm the uniformity of coastal water composition in terms of metal concentrations.
The present study reveals higher concentrations of all the heavy elements studied (except for Zn) for the mullets caught from the Black Sea (Bulgaria) compared to those from the Ionian Sea (Italy).
Several authors have previously investigated the feeding habits and heavy metal distributions in grey mullet (M. cephalus), since this fish species lives close to the bottom sediments [55,56,57,58,59]. They found that the mullet specimens accumulate heavy metals in various tissues, and this is a prominent indicator for the heavy metal pollution coming from the surrounding water bodies.
The levels of metals in the tissues of grey mullet collected in different regions may indicate the current pollution status concerning the metals of the area where the fish are caught. Our results provide useful information on the distribution of metals in the muscle, gills, and liver of grey mullet caught in the Black Sea and the Ionian Sea. They indicated that metals have a different degree of accumulation in different tissues of this species and in specimens coming from different localities, confirming that geographical locations can determine different metal concentrations in the same fish species, as previously documented by several authors [2,37].

5. Conclusions

The present study provides novel information about the distribution of heavy metals in M. cephalus and marine water collected from two different European regions—the Black Sea (Bulgaria) and the Ionian Sea (Italy). The results from the study show that the different accumulation levels of the analyzed metals in various tissues of M. cephalus caught from the Black Sea (Bulgaria) and the Ionian Sea (Italy) might be used as good tool for coastal water monitoring, independently of the coastal area.
Moreover, the present paper attempts to define a baseline dataset for M. cephalus muscle tissue metal concentrations for both environmental and fish health.
Additionally, the results from this study may serve as a convenient approach during the marine environmental monitoring and pollution programs set by both countries (Italy and Bulgaria).

Author Contributions

Conceptualization, F.F., G.C., and L.M.; methodology, C.S. and K.P.; data curation, F.F. and G.C.; software, C.D. and C.S.; validation, G.P., F.F., and L.M.; formal analysis, C.S., C.D., and K.P.; writing—original draft preparation, C.D., C.S., F.F., and G.C.; writing—review and editing, G.P. and K.P.; supervision, L.M., G.P., and F.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Argamino, C.R.; Janairo, J.I.B. Qualitative assessment and management of microplastics in Asian green mussels (Perna viridis) cultured in Bacoor Bay, Cavite, Phillipines. Environ. Asia 2016, 9, 48–54. [Google Scholar]
  2. Bahnasawy, M.; Khidr, A.A.; Dheina, N. Seasonal variations of heavy metals concentrations in mullet, Mugil cephalus and Liza ramada (Mugilidae) from Lake Manzala, Egypt. Egypt. J. Aquat. Boil. Fish. 2009, 13, 81–100. [Google Scholar] [CrossRef]
  3. Bat, L.; Sezgin, M.; Üstün, F.; Şahin, F. Heavy metal concentrations in ten species of fishes caught in Sinop coastal waters of the Black Sea, Turkey. Turk. J. Fish. Aquat. Sci. 2012, 12, 371–376. [Google Scholar] [CrossRef]
  4. Marcovecchio, J.; Marcovecchio, J.E. The use of Micropogonias furnieri and Mugil liza as bioindicators of heavy metals pollution in La Plata river estuary, Argentina. Sci. Total. Environ. 2004, 323, 219–226. [Google Scholar] [CrossRef]
  5. Phillips, D.J.; Segar, D.A. Use of bio-indicators in monitoring conservative contaminants: Programme design imperatives. Mar. Pollut. Bull. 1986, 17, 10–17. [Google Scholar] [CrossRef]
  6. Atta, A.; Voegborlo, R.B.; Agorku, E.S. Total mercury distribution in different tissues of six species of freshwater fish from the Kpong hydroelectric reservoir in Ghana. Environ. Monit. Assess. 2011, 184, 3259–3265. [Google Scholar] [CrossRef]
  7. Canli, M.; Atli, G. The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and the size of six Mediterranean fish species. Environ. Pollut. 2003, 121, 129–136. [Google Scholar] [CrossRef]
  8. Muñoz-Olivas, R.; Cámara, C. Speciation related to human health. Trace Elem. Speciat. Environ. Food Health 2007, 331–353. [Google Scholar] [CrossRef]
  9. García-González, C.A.; Alnaief, M.; Smirnova, I. Polysaccharide-based aerogels—Promising biodegradable carriers for drug delivery systems. Carbohydr. Polym. 2011, 86, 1425–1438. [Google Scholar] [CrossRef]
  10. Govind, P. Heavy Metals Causing Toxicity in Animals and Fishes. Res. J. Anim. Res. J. Anim. Vet. Fish. Sci. Int. Sci. Congr. Assoc. 2014, 2, 17–23. [Google Scholar]
  11. Sfakianakis, D.G.; Renieri, E.; Kentouri, M.; Tsatsakis, A. Effect of heavy metals on fish larvae deformities: A review. Environ. Res. 2015, 137, 246–255. [Google Scholar] [CrossRef]
  12. Montalbano, G.; Capillo, G.; Laura, R.; Abbate, F.; Levanti, M.; Guerrera, M.; Ciriaco, E.; Germana, A. Neuromast hair cells retain the capacity of regeneration during heavy metal exposure. Ann. Anat. Anat. Anz. 2018, 218, 183–189. [Google Scholar] [CrossRef]
  13. Costa, R.; Albergamo, A.; Piparo, M.; Zaccone, G.; Capillo, G.; Manganaro, A.; Dugo, P.; Mondello, L. Multidimensional gas chromatographic techniques applied to the analysis of lipids from wild-caught and farmed marine species. Eur. J. Lipid Sci. Technol. 2016, 119, 1600043. [Google Scholar] [CrossRef]
  14. Fazio, F.; Saoca, C.; Sanfilippo, M.; Capillo, G.; Spanò, N.; Piccione, G. Response of vanadium bioaccumulation in tissues of Mugil cephalus (Linnaeus 1758). Sci. Total. Environ. 2019, 689, 774–780. [Google Scholar] [CrossRef] [PubMed]
  15. Çelik, U.; Oehlenschläger, J. Determination of zinc and copper in fish samples collected from Northeast Atlantic by DPSAV. Food Chem. 2004, 87, 343–347. [Google Scholar] [CrossRef]
  16. Schroeder, H.A. The trace elements and man; Dodd Mead: New York, NY, USA, 1973; pp. 171. [Google Scholar]
  17. Ihunwo, O.C.; Dibofori-Orji, A.N.; Olowo, C.; Ibezim-Ezeani, M.U. Distribution and risk assessment of some heavy metals in surface water, sediment and grey mullet (Mugil cephalus) from contaminated creek in Woji, southern Nigeria. Mar. Pollut. Bull. 2020, 154, 111042. [Google Scholar] [CrossRef] [PubMed]
  18. Makedonski, L.; Peycheva, K.; Stancheva, M. Determination of heavy metals in selected black sea fish species. Food Control. 2017, 72, 313–318. [Google Scholar] [CrossRef]
  19. Peycheva, K.; Panayotova, V.; Merdzhanova, A.; Stancheva, R. Estimation of THQ and potential health risk for metals by comsumption of some black sea marine fishes and mussels in Bulgaria. Bulg. Chem. Commun. 2019, 51, 241–246. [Google Scholar]
  20. Soyinka, O.O. The feeding ecology of Mugil cephalus (Linnaeus) from a high brackish tropical lagoon in South-west, Nigeria. Afr. J. Biotechnol. 2008, 7, 4192–4198. [Google Scholar]
  21. Turkmen, M.; Turkmen, A.; Tepe, Y. Metal contaminations in five fish species from black, marmara, aegean and mediterranean seas, turkey. J. Chil. Chem. Soc. 2008, 53, 1424–1428. [Google Scholar] [CrossRef]
  22. Stoichev, T.; Makedonski, L.; Trifonova, T.; Stancheva, M.; Ribarova, F. DDT in fish from the Bulgarian region of the Black Sea. Chem. Ecol. 2007, 23, 191–200. [Google Scholar] [CrossRef]
  23. Brandt, P.; Rubino, A.; Quadfasel, D.; Alpers, W.; Sellschopp, J.; Fiekas, H.V. Evidence for the influence of Atlantic-Ionian Stream fluctuations on the tidally induced internal dynamics in the Strait of Messina. J. Phys. Oceanogr. 1999, 29, 1071–1080. [Google Scholar] [CrossRef]
  24. Grandjacquet, C.; Mascle, G. The Structure of the Ionian Sea, Sicily, and Calabria-Lucania. In The Ocean Basins and Margins; Nairn, A.E.M., Kanes, W.H., Stehli, F.G., Eds.; Springer US: Boston, MA, USA, 1978; pp. 257–329. [Google Scholar]
  25. Bottari, A.; Carveni, P.; Giacobbe, S.; Spanò, N.; Bottari, C. Genesis and geomorphologic and ecological evolution of the Ganzirri salt marsh (Messina, Italy). Quat. Int. 2005, 150–158. [Google Scholar] [CrossRef]
  26. Capillo, G.; Savoca, S.; Costa, R.; Sanfilippo, M.; Rizzo, C.; Giudice, A.L.; Albergamo, A.; Rando, R.; Bartolomeo, G.; Spanò, N.; et al. New Insights into the Culture Method and Antibacterial Potential of Gracilaria gracilis. Mar. Drugs 2018, 16, 492. [Google Scholar] [CrossRef]
  27. Manganaro, A.; Pulicanò, G.; Sanfilippo, M. Temporal evolution of the area of Capo Peloro (Sicily, Italy) from pristine site into urbanized area. Transit. Waters Bull. 2011, 5, 23–31. [Google Scholar]
  28. Lermusiaux, P.; Robinson, A. Features of dominant mesoscale variability, circulation patterns and dynamics in the Strait of Sicily. Deep. Sea Res. Part I Oceanogr. Res. Pap. 2001, 48, 1953–1997. [Google Scholar] [CrossRef]
  29. Iaria, C.; Saoca, C.; Guerrera, M.C.; Ciulli, S.; Brundo, M.V.; Piccione, G.; Lanteri, G. Occurrence of diseases in fish used for experimental research. Lab. Anim. 2019, 53, 619–629. [Google Scholar] [CrossRef]
  30. European Parliament and Council of the European Union. Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the Protection of Animals Used for Scientific Purposes; European Parliament and Council of the European Union: Brussels, Belgium, 2013. [Google Scholar]
  31. Kojadinovic, J.; Potier, M.; Le Corre, M.; Cosson, R.P.; Bustamante, P. Bioaccumulation of trace elements in pelagic fish from the Western Indian Ocean. Environ. Pollut. 2007, 146, 548–566. [Google Scholar] [CrossRef]
  32. Dang, F.; Wang, W.-X. Assessment of tissue-specific accumulation and effects of cadmium in a marine fish fed contaminated commercially produced diet. Aquat. Toxicol. 2009, 95, 248–255. [Google Scholar] [CrossRef]
  33. Farkas, A.; Salánki, J.; Specziár, A. Age- and size-specific patterns of heavy metals in the organs of freshwater fish Abramis brama L. populating a low-contaminated site. Water Res. 2003, 37, 959–964. [Google Scholar] [CrossRef]
  34. Doraghi, A.; Monikh, F.A.; Safahieh, A.; Savari, A. Heavy Metals Concentration in Mullet Fish, from Petrochemical Waste Receiving Creeks, Musa Estuary (Persian Gulf). J. Environ. Prot. 2011, 2, 1218–1226. [Google Scholar] [CrossRef]
  35. Türkmen, M.; Ciminli, C. Determination of metals in fish and mussel species by inductively coupled plasma-atomic emission spectrometry. Food Chem. 2007, 103, 670–675. [Google Scholar] [CrossRef]
  36. Sidoumou, Z.; Gnassia-Barelli, M.; Siau, Y.; Morton, V.; Roméo, M. Distribution and Concentration of Trace Metals in Tissues of Different Fish Species from the Atlantic Coast of Western Africa. Bull. Environ. Contam. Toxicol. 2005, 74, 988–995. [Google Scholar] [CrossRef] [PubMed]
  37. Uysal, K. Heavy metal in edible portions (muscle and skin) and other organs (gill, liver and intestine) of selected freshwater fish species. Int. J. Food Prop. 2011, 14, 280–286. [Google Scholar] [CrossRef]
  38. Eken, M.; Göksu, M.Z.L.; Özak, A.A. Investigation of heavy metal levels in economically important fish species captured from the Tuzla lagoon. Food Chem. 2007, 102, 415–421. [Google Scholar] [CrossRef]
  39. Company, R.; Felícia, H.; Serafim, M.A.P.; Almeida, A.; Biscoito, M.J.; Bebianno, M.J. Metal concentrations and metallothionein-like protein levels in deep-sea fishes captured near hydrothermal vents in the Mid-Atlantic Ridge off Azores. Deep. Sea Res. Part I Oceanogr. Res. Pap. 2010, 57, 893–908. [Google Scholar] [CrossRef]
  40. Kraemer, L.D.; Campbell, P.G.C.; Hare, L. Seasonal variations in hepatic Cd and Cu concentrations and in the sub-cellular distribution of these metals in juvenile yellow perch (Perca flavescens). Environ. Pollut. 2006, 142, 313–325. [Google Scholar] [CrossRef]
  41. Jezierska, B.; Witeska, M. The Metal Uptake and Accumulation in Fish Living in Polluted Waters. In Soil and Water Pollution Monitoring, Protection and Remediation; Springer: Dordrecht, The Netherlands, 2007; pp. 107–114. [Google Scholar]
  42. Karadede, H.; Oymak, S.A.; Ünlü, E. Heavy metals in mullet, Liza abu, and catfish, Silurus triostegus, from the Atatürk Dam Lake (Euphrates), Turkey. Environ. Int. 2004, 30, 183–188. [Google Scholar] [CrossRef]
  43. Al-Yousuf, M.; El-Shahawi, M.; Al-Ghais, S. Trace metals in liver, skin and muscle of Lethrinus lentjan fish species in relation to body length and sex. Sci. Total. Environ. 2000, 256, 87–94. [Google Scholar] [CrossRef]
  44. Lima, R.G.D.S.; Araújo, F.G.; Maia, M.F.; Pinto, A.S.D.S.B.; Junior, R.G.D.S.L. Evaluation of Heavy Metals in Fish of the Sepetiba and Ilha Grande Bays, Rio de Janeiro, Brazil. Environ. Res. 2002, 89, 171–179. [Google Scholar] [CrossRef]
  45. Usero, J.; Izquierdo, C.; Morillo, J.; Gracia, I. Heavy metals in fish (Solea vulgaris, Anguilla anguilla and Liza aurata) from salt marshes on the southern Atlantic coast of Spain. Environ. Int. 2004, 29, 949–956. [Google Scholar] [CrossRef]
  46. Allen-Gil, S.; Martynov, V. Heavy metal burdens in nine species of freshwater and anadromous fish from the Pechora River, northern Russia. Sci. Total. Environ. 1995, 653–659. [Google Scholar] [CrossRef]
  47. Morel, F.M.M.; Kraepiel, A.M.L.; Amyot, M. The chemical cycle and bioaccumulation of mercury. Annu. Rev. Ecol. Syst. 1998, 29, 543–566. [Google Scholar] [CrossRef]
  48. Boran, M.; Altinok, I. A review of heavy metals in water, sediment and living organisms in the black sea. Turk. J. Fish. Aquat. Sci. 2010, 10, 565–572. [Google Scholar]
  49. Wang, W.-X. Bioaccumulation and Biomonitoring. In Marine Ecotoxicology; Elsevier BV: Amsterdam, The Netherlands, 2016; pp. 99–119. [Google Scholar]
  50. Savoca, S.; Grifó, G.; Panarello, G.; Albano, M.; Giacobbe, S.; Capillo, G.; Spanó, N.; Consolo, G. Modelling prey-predator interactions in Messina beachrock pools. Ecol. Model. 2020, 434, 109206. [Google Scholar] [CrossRef]
  51. Costa, R.; Capillo, G.; Albergamo, A.; Volsi, R.L.; Bartolomeo, G.; Bua, G.; Ferracane, A.; Savoca, S.; Gervasi, T.; Rando, R.; et al. A Multi-screening Evaluation of the Nutritional and Nutraceutical Potential of the Mediterranean Jellyfish Pelagia noctiluca. Mar. Drugs 2019, 17, 172. [Google Scholar] [CrossRef]
  52. Spinelli, A.; Capillo, G.; Faggio, C.; Vitale, D.; Spanò, N. Returning of Hippocampus hippocampus (Linnaeus, 1758) (Syngnathidae) in the Faro Lake–oriented Natural Reserve of Capo Peloro, Italy. Nat. Prod. Res. 2018, 34, 595–598. [Google Scholar] [CrossRef]
  53. Capillo, G.; Panarello, G.; Savoca, S.; Sanfilippo, M.; Albano, M.; Volsi, R.L.; Consolo, G.; Spanò, N. Intertidal ponds of messina’s beachrock faunal assemblage, evaluation of ecosystem dynamics and communities’ interactions. AAPP Atti Accad. Peloritana Pericolanticl. Sci. Fis. Mat. Nat. 2018, 96, A41–A416. [Google Scholar]
  54. Pan, K.; Wang, W.-X. Validation of Biokinetic Model of Metals in the Scallop Chlamys nobilis in Complex Field Environments. Environ. Sci. Technol. 2008, 42, 6285–6290. [Google Scholar] [CrossRef]
  55. Agamy, N.; Gomaa, A. Heavy Metals and Chemical Composition of Mullet Fish and Water Quality of Its Farms. J. High Inst. Public Health 2012, 42, 63–81. [Google Scholar] [CrossRef]
  56. Fazio, F.; Piccione, G.; Tribulato, K.; Ferrantelli, V.; Giangrosso, G.; Arfuso, F.; Faggio, C. Bioaccumulation of Heavy Metals in Blood and Tissue of Striped Mullet in Two Italian Lakes. J. Aquat. Anim. Health 2014, 26, 278–284. [Google Scholar] [CrossRef] [PubMed]
  57. Mendis, B.R.C.; Najim, M.; Kithsiri, H.M.P.; Azmy, S.A.M. Bioaccumulation of Heavy Metals in the Selected Commercially Important Edible Fish Species Gray Mullet (Mugil cephalus) from Negombo Estuary. J. Environ. Prof. Sri Lanka 2015, 4. [Google Scholar] [CrossRef]
  58. Priya, S.L.; Selvam, A.P.; Purvaja, R.; Senthilkumar, B.; Hariharan, G.; Ramesh, R. Bioaccumulation of heavy metals in mullet ( Mugil cephalus ) and oyster ( Crassostrea madrasensis ) from Pulicat lake, south east coast of India. Toxicol. Ind. Health 2010, 27, 117–126. [Google Scholar] [CrossRef]
  59. Stancheva, M.; Makedonski, L.; Petrova, E. Determination of heavy metals (Pb, Cd, As and Hg) in Black Sea grey mullet (Mugil cephalus). Bulg. J. Agric. Sci. 2013, 1, 30–34. [Google Scholar]
Figure 1. Maps indicating different sampling points. (A) Central-eastern Mediterranean Sea. (B) Ionian Sea (Italy) (sampling stations I1, I2, T3), (C) Black Sea (Bulgaria) (sampling stations B1, B2, B3).
Figure 1. Maps indicating different sampling points. (A) Central-eastern Mediterranean Sea. (B) Ionian Sea (Italy) (sampling stations I1, I2, T3), (C) Black Sea (Bulgaria) (sampling stations B1, B2, B3).
Animals 10 01739 g001
Figure 2. Metal concentration in different tissues of Mugil cephalus (Linnaeus, 1758) from the Ionian Sea, Italy. Different alphabetical characters represent statistical differences (p < 0.05). From (AI) are plotted metal concentrations in the following order: Cd, Cr, Pb, Ni, Al, Cu, Fe, Mn, and Zn.
Figure 2. Metal concentration in different tissues of Mugil cephalus (Linnaeus, 1758) from the Ionian Sea, Italy. Different alphabetical characters represent statistical differences (p < 0.05). From (AI) are plotted metal concentrations in the following order: Cd, Cr, Pb, Ni, Al, Cu, Fe, Mn, and Zn.
Animals 10 01739 g002
Figure 3. Metal concentrations in different tissues of Mugil cephalus (Linnaeus, 1758) from the Black Sea, Bulgaria. Different alphabetical characters represent statistical differences (p < 0.05). From (AI) are plotted metal concentrations in the following order: Cd, Cr, Pb, Ni, Al, Cu, Fe, Mn, and Zn.
Figure 3. Metal concentrations in different tissues of Mugil cephalus (Linnaeus, 1758) from the Black Sea, Bulgaria. Different alphabetical characters represent statistical differences (p < 0.05). From (AI) are plotted metal concentrations in the following order: Cd, Cr, Pb, Ni, Al, Cu, Fe, Mn, and Zn.
Animals 10 01739 g003
Table 1. Biometrics data (mean ± SD) of the grey mullet sampled from the coastal waters of the Black Sea (Bulgaria) and the Ionian Sea (Italy).
Table 1. Biometrics data (mean ± SD) of the grey mullet sampled from the coastal waters of the Black Sea (Bulgaria) and the Ionian Sea (Italy).
SampleSampling
Site
NSampling
Stations
Weight
(g) ± SD
Length
(cm) ± SD
Gray mullet (Mugil cephalus)Black Sea
(Bulgaria)
20B1, B2, B3104.33 ± 13.8023.17 ± 2.61
Ionian Sea
(Italy)
20I1, I2, I397.12 ± 11.2522.41 ± 2.38
SD: Standard Deviation.
Table 2. Trace element concentration (mean ± SD) measured in the seawater of the Black Sea (Bulgaria) and the Ionian Sea (Italy).
Table 2. Trace element concentration (mean ± SD) measured in the seawater of the Black Sea (Bulgaria) and the Ionian Sea (Italy).
Trace Elements (μg/L)Sampling Sites
Black Sea (Bulgaria)Ionian Sea (Italy)
Cd0.0445 ± 0.00200.9289 ± 0.0095 *
Cr0.3751 ± 0.00440.9042 ± 0.0148 *
Pb0.3472 ± 0.00060.8060 ± 0.1095 *
Ni0.5286 ± 0.01130.8435 ± 0.0440 *
Al5.4634 ± 0.22080.9350 ± 0.0215 *
Cu0.5340 ± 0.008041.2700 ± 0.2720 *
Fe3.4591 ± 0.18340.8920 ± 0.0507 *
Mn0.5388 ± 0.03070.9385 ± 0.0048 *
Zn22.1829 ± 0.10490.8821 ± 0.0379 *
* Shows significance (p < 0.0001); SD: Standard Deviation.
Table 3. Trace element concentrations (mean ± SD) of the various tissues measured in the grey mullet Mugil cephalus (Linnaeus, 1758) caught from the Ionian Sea (Italy) and the Black Sea (Bulgaria).
Table 3. Trace element concentrations (mean ± SD) of the various tissues measured in the grey mullet Mugil cephalus (Linnaeus, 1758) caught from the Ionian Sea (Italy) and the Black Sea (Bulgaria).
Heavy metals (μg/L)SamplesMuscleGillsLiver
CdIonian Sea0.0008 ± 0.0010 a0.0034 ± 0.0021 a0.0351 ± 0.0217 a
Black Sea0.0391 ± 0.0043 b0.0214 ± 0.0058 b0.2391 ± 0.0034 b
CrIonian Sea 0.0213 ± 0.0012 a0.0602 ± 0.0106 a0.1506± 0.0066 a
Black Sea 0.1809 ± 0.0051 b0.3340 ± 0.0678 b0.1303 ± 0.0027 b
PbIonian Sea0.0572 ± 0.0104 a0.5320 ± 0.0844 a0.1970 ± 0.0771 a
Black Sea0.1914 ± 0.0046 b2.768 ± 0.0525 b0.5118 ± 0.0098 b
NiIonian Sea 0.0071 ± 0.0011 a0.0610 ± 0.0079 a0.1735± 0.0315 a
Black Sea0.1249 ± 0.0211 b0.2144 ± 0.0033 b0.2111 ± 0.0062 b
AlIonian Sea 4.8500 ± 0.8082 a9.0230 ± 0.7341 a20.2900 ± 1.9230 a
Black Sea1.0210 ± 0.0061 b47.3800 ± 2.5700 b33.3100 ± 0.4651 b
CuIonian Sea 0.2695 ± 0.0473 a0.7400 ± 0.1114 a0.6600 ± 0.1635 a
Black Sea1.8270 ± 0.0151 b1.1760 ± 0.0385 b68.6200 ± 0.3200 b
FeIonian Sea 5.9250 ± 0.9792 a54.9100 ± 5.1440 a33.1500 ± 3.2970 a
Black Sea11.0600 ± 1.6310 b50.8900 ± 1.6730 b502.3000 ± 2.0410 b
MnIonian Sea 0.3040 ± 0.0484 a7.8550 ± 0.9310 a1.5350 ± 0.2455 a
Black Sea0.1376 ± 0.0183 b30.3300 ± 0.7803 b1.6710 ± 0.0204 b
ZnIonian Sea 19.3000 ± 2.0800 a19.6000 ± 1.7890 a30.0000 ± 1.8920 a
Black Sea4.5330 ± 0.5551 b18.1100 ± 0.7027 b18.4800 ± 0.4849 b
Means without the same alphabetical characters (a, b) within the same parameter and tissue represent statistical differences (p < 0.0001).
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