Volume 9 - 2022 | https://doi.org/10.3389/fmars.2022.899555
This article is part of the Research TopicAdvances in the Environmental Distribution of Less Studied ElementsView all 5 articles
This study aimed at assessing the accumulation of some trace elements (arsenic
and zinc) in the soft tissue of Mediterranean mussels (Mytilus galloprovincialis) from the Black Sea
The mussel samples were collected on a monthly basis between February and June 2019 from two stations located in front of the Danube–Black Sea Canal lock
The mussels (260 samples) were divided into three classes according to their length: A (3−5.9 cm)
The concentrations (dry basis) of As (12.5 ± 3.0 mg/kg)
and Zn (179.5 ± 2.5 mg/kg) were determined using spectrometric techniques
The mean daily values of the physicochemical parameters of seawater (temperature
and dissolved oxygen content) within the study area were reported
Higher element concentrations were generally found for mussels from size classes A and B compared with those of the larger and older mussels from class C
Principal component analysis (PCA) suggested that the phytoplankton represented an important source of As and Br for the smaller mussels collected in February (when the levels of seawater temperature were lower and those of pH and salinity higher) compared to the larger mussels collected in June
the multivariate analysis suggested that Cu
and Br originated from similar anthropogenic sources and their higher concentrations reported in February and June were obtained at lower levels of seawater salinity
and Hg in the mussel soft tissue were lower than the maximum permissible levels
Due to their tendency to accumulate in living tissues and toxicity potential, trace elements (TEs) have been a major concern for the marine environment in recent years (Belivermis et al., 2016). They enter the aquatic ecosystem, accumulate in aquatic organisms, e.g., fish, mollusks, algae, and are transferred to people through consumption. Consequently, TEs pose a risk to the health of the ecosystem and humans (Çevik et al., 2008)
Essential elements are toxic at high concentrations
whereas non-essential ones are toxic even at very low concentrations
Mussel samples were collected from two points, i.e., stations A and B, located in front of the Danube–Black Sea Canal lock, along the two artificial dikes within the outer berths of Agigea Port (Figure 1)
Stations A and B are 2.7 km and 2.3 km
The mean water depth in the study area was about 8 m
Figure 1 Constanta Sud−Agigea Port area map (Google Earth Pro 7.3.4.8248, 2021; http://earth.google.com)
Agigea Port represents the southern limit of Constanta Port
the most important industrial and maritime hub on the Romanian Black Sea coast
the study area is characterized by strong anthropogenic pressures resulting from intense port activities
Important cargo quantities are carried through the Danube–Black Sea Canal
and food are dealt with at specialized terminals in the port
The mussels were randomly collected from their artificial rocky substrate (dyke) by scuba divers between February and June 2019
Similar environmental conditions for the mussels collected from the two sampling stations were assumed
given the relatively short distance between the dykes (0.4 km)
The samples were stored in a freezer (-20°C) until further analysis
Prior to processing for spectrometric analyses
a series of biometric measurements were performed
The length (L) and wet mass (mw) of each mussel (after thawing and removing the excess water by blotting) were measured using a caliper and an analytical balance (Kern
The mussels were classified into the following groups according to their length: A (L=3–5.9 cm)
Similar growth rates and ages were assumed for mussels from each size class
20 samples/class/month × 3 classes (A–C) × 3 months (February–April) and 20 samples/class/month × 2 classes (A and B) × 2 months (May and June)
were dissected with a scalpel to separate the soft tissue from the shell
Flesh samples were weighed (after removing the excess intervalvar liquid by blotting)
freeze-dried at -55°C for 48 h using a freeze-dryer (ilShin BioBase
The meat yield (MY) was calculated using Eq
where mwf represents the mass of wet flesh and mw is the mass of wet mussel (flesh and shell)
Table 1 Comparison between measured and certified values of element concentration in standard reference materials
The mean daily values of the physicochemical parameters of seawater, in terms of the temperature (t), salinity (S), pH (pH), chlorophyll a concentration (cc), and dissolved oxygen concentration (cDO), within the study area were taken from the Copernicus Marine Environment Monitoring Service Platform
The physicochemical properties of the water (t
and concentrations of the TEs in the mussel soft tissue (ci
The dissolved O2 concentrations (cDO=289−357 mmol/m3) varied significantly between and within the months
Higher values (330−357 mmol/m3) were in the colder periods (lower seawater temperature
Higher levels of cDO in February−April corresponded to those of cc
Figure 2 Time variation of mean daily values of seawater temperature (t)
and dissolved oxygen concentration (cDO) in February–June 2019
Variations in the wet flesh mass (mwf=5.1−23.4 g) and meat yield (MY=34.1−69.5%) between February and June 2019, which are shown in Figure 3
highlight the following issues: (i) for individuals from class A
the mwf (5.1−9.1 g) decreased slightly from February to May and the value of mwf in June was 1.80 times higher than that in May; the MY (34.6−69.5%) increased slightly from February to April
the values of MY in April and May were almost equal (≈41%)
and the value of MY in June was 1.71 times higher than that in May; (ii) for individuals from class B
the mwf (8.6−14.8 g) exhibited an increase in March (1.36 times)
and a smaller decrease in June (1.16 times); the MY (34.1−40.2%) increased slightly until April
the values of MY in April and May were almost equal (≈37%)
and the value of MY in June was 1.08 times lower than that in May; (iii) for individuals from class C
the mwf (15.8−23.4 g) increased from February to April; the MY (35.1−41.7%) increased until April and the increase was most significant in March (1.15 times)
Figure 3 Variation of wet flesh mass (mwf) and meat yield (MY) in February−June 2019 for individuals from size classes A
Figure 4 Levels of monthly concentration of trace elements in the soft tissue of mussel classes A
Figure 5 PCA bi-plot (projections of variables and samples on the factor-plane PC1−PC2)
as well as a strong negative correlation between cDO and t (r=-0.78)
The following mussel gametogenesis stages were reported for M. galloprovincialis (Ciocan, 2002; Suarez et al., 2005; Okaniwa et al., 2010; Bhaby et al., 2014; Azpeitia et al., 2017; Rouabhi et al., 2019): (i) 0 - sexual rest and accumulation of reserve substances (glycogen
proteins) in adipogranular (ADG) and vesicular connective tissue (VCT) cells; (ii) I - beginning of gametogenesis (multiplication of gonia
development of follicles); (iii) II - gamete development (immature ovules and spermatozoa
more apparent follicles); (iv) IIIa - gamete maturation (gonadal follicles full of mature gametes); (v) IIIb - spawning (gamete release); (vi) IIIc - gamete restoration; (vii) IIId - follicle cleaning process (gamete degradation)
Based on data from the literature (Ciocan, 2002; Suarez et al., 2005; Okaniwa et al., 2010; Bhaby et al., 2014; Vasechkina and Kazankova, 2014; Azpeitia et al., 2017; Rouabhi et al., 2019), the results presented in Figure 3 suggest the following issues: (i) for the smaller and younger mussels from class A
a sexual rest phase (0) is characteristic for the period of February−May
which suggests that immature specimens (up to 1 year old) are predominant; moreover
an early development phase (I) could occur at the end of this period; the significant increase in the flesh mass in June could be an effect of the gamete development and maturation phases (II and IIIa)
and of favorable environmental factors (mainly higher temperatures and lower levels of salinity); (ii) for mussels from class B
the gamete development and maturation phases (II and IIIa) occur in February and March
followed by a first (intense) spawning phase (IIIb) in April
and a second (slightly less intense) spawning phase (IIIb) in June; (iii) for the larger and older mussels from class C
the gamete development and maturation phases (II and IIIa) occur in the period of February−April (it is possible only in March and April)
and are most likely followed by a spawning phase (IIIb) in May
suggesting the possibility of similar sources of intake
The PC1 coordinates of group MS1 (samples A
correspond to lower values of t (5°C) and MY (34.14−35.14%)
PC1 coordinates of group MS5 (samples A and B collected in June)
correspond to higher values of t (22°C) and MY (69.46% for A5 class)
PC2 can discriminate between the samples collected in February and June (groups MS1 and MS5 with PC2 coordinates of 0.90−2.72)
which generally had higher values of cBr (152−309 mg/kg)
and those collected in March−May (groups MS2−MS4 with PC2 coordinates between -2.12 and -0.33)
which had lower values of cBr (124−195 mg/kg)
PCA emphasizes that PC1 is positively associated with cAs
as well as negatively associated with t and MY
This indicates that the phytoplankton was an important source of As and Br for the smaller mussels collected in February (group MS1) compared to the larger ones collected in June (group MS5)
Referring to the mean (m) values of seawater properties
lower levels of tm (5°C) as well as higher levels of pHm (8.38) and Sm (15.5 PSU) were reached in February compared to June (tm=22 °C
and Br originated from similar anthropogenic sources and their higher concentrations reported in February and June were obtained at lower levels of S
corresponding to higher flow rates of the Danube in these two months
whereas the values of cBr (124−309 mg/kg) were quite similar
Table 3 Concentrations (dry basis) of some trace elements in the soft tissue of M
Where available, the element concentrations obtained in this study (wet basis) were compared with the maximum permissible levels (MPLs) (Wagner and Boman, 2003; Wagner and Boman, 2004; EC 1881, 2006) (Supplementary Table S4)
The values of cCu (0.841−1.777 mg/kg)
and cHg (0.001−0.008 mg/kg) were lower than their corresponding MPLs
The current study provides new information on the concentration of some TEs
galloprovincialis mussels collected from an artificial rocky substrate (Agigea Port
The order of accumulation was as follows: Zn>Br>As>Cu>Se>Hg
Different element bioaccumulation patterns were identified within the three classes of mussel length
Higher element concentrations were generally found for the mussels from classes A and B compared to the larger and older mussels from class C
The variables used in multivariate analysis were as follows: seawater temperature (t=4−24°C)
chlorophyll a concentration (cc=0.1−6 mg/m3)
dissolved oxygen concentration (cDO=289−357 mmol/m3)
concentrations (dry basis) of As (cAs=9.22−19.3 mg/kg)
The MY was positively correlated with t and negatively correlated with pH
The results of PCA indicated the following relevant issues: (i) PC1 was positively associated with cAs
as well as negatively associated with t and MY; this suggests that the phytoplankton represented an important source of As and Br for the smaller mussels collected in February (when the levels of t were lower and those of pH and S higher) compared to the larger mussels collected in June; (ii) PC2 was positively associated with cCu
and Br originated from similar sources (e.g.
wastewater discharges) and their higher concentrations reported in February and June were obtained at lower levels of S (corresponding to higher flow rates of the Danube)
The concentrations of As, Cu, Hg, and Zn fall in the range of those found in low to moderately polluted areas. The levels of cHg, i.e., 0.001−0.008 mg/kg (wet basis), were much lower than the maximum permissible level specified in EC 1881 (2006)
temporal variations of concentrations of Br and Se were reported
Few studies on mussels from the Black Sea have focused on the assessment of Br and Se bioaccumulation
The information provided may be useful in supplementing existing data on TE pollution in the Black Sea
The original contributions presented in the study are included in the article/Supplementary Material
Further inquiries can be directed to the corresponding authors
OP and DV had a substantial contribution to the conception of article
AB and MM performed and described the experimental part
All authors contributed to the article and approved the submitted version
The study was financially supported by the Romanian Ministry of Research
Innovation and Digitization in the framework of the national CORE Program (projects PN 19200302 and 19200102) and PFE/2021 “Research of excellence for pointing out environmental and biotical changes in ancient and recent aquatic systems−AMBIACVA
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations
Any product that may be evaluated in this article
or claim that may be made by its manufacturer
is not guaranteed or endorsed by the publisher
The authors thank SCECB “Natura Z” Association for providing M
galloprovincialis samples collected by scuba divers
the habitat destruction being carefully avoided
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmars.2022.899555/full#supplementary-material
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Received: 18 March 2022; Accepted: 02 May 2022;Published: 01 June 2022
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