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Heavy metals in some commercially fishery products marketed in Saudi Arabia

Abstract

Seven major commercially important marine fisheries species, Fenneropenaeus indicus, Chaceon quinquedens, Lethrinus nebulosus, Scomberomorus commerson, Plectropomus pessuliferus, Pampus argenteus, and Epinephelus summana were seasonally sampled from Jeddah main local fisheries market, Saudi Arabia. The heavy metals, namely arsenic (As), cadmium (Cd), chromium (Cr), cobalt (Co), copper (Cu), iron (Fe), lead (Pb), nickel (Ni), and zinc (Zn) were assessed. Except for arsenic, the results indicated that the levels of tested heavy elements were within the standard limits. The levels of arsenic were high in F. indicus, C. quinquedens, L. nebulosus, P. pessuliferus and E. summana. In addition, Pb showed higher mean levels of 0.89 ± 0.14 mg/kg and 5.05 ± 0.86 mg/kg in S. commerson and P. pessuliferus, respectively, compared to the permissible standard limits. Cd was not found in most samples, except for F. indicus and C. quinquedens where its detected levels exceeded the acceptable standards. Our results may prove the significant roles of seasonal impacts and species variations in the acquisition mechanisms of heavy metals in marine environments. Therefore, the application of a detection program for cumulative residual levels of heavy metals in marine fisheries products is recommended before marketing to ensure the safety of these products.

Keywords:
marine water; marine species; heavy metals; standard parameters

1 Introduction

Heavy metals are the major environmental pollutants in the air, water, and soil. Their existence at high levels in the environment is hazardous to human health due to their high toxic impacts on living bodies (Alnashiri, 2022Alnashiri, H. M. (2022). A brief review on heavy metal bioaccumulation studies from Red Sea. Adsorption Science and Technology, 2022, 6201299. http://dx.doi.org/10.1155/2022/6201299.
http://dx.doi.org/10.1155/2022/6201299...
). Heavy metal contamination in the marine environment is of deep concern as it negatively affects marine and human lives. Factors such as anthropogenic activities, industrialization, and urbanization are the main causes of pollution in the marine environment worldwide (Mahboob et al., 2022Mahboob, S., Ahmed, Z., Khan, M. F., Virik, P., Al-Mulhm, N., & Baabbad, A. A. A. (2022). Assessment of heavy metals pollution in seawater and sediments in the Arabian Gulf, near Dammam, Saudi Arabia. Journal of King Saud University – Science, 34(1), 101677. http://dx.doi.org/10.1016/j.jksus.2021.101677.
http://dx.doi.org/10.1016/j.jksus.2021.1...
). In the Arabian Gulf area of Saudi Arabia, the wastes of refineries and the petrochemical industry are the main sources of heavy metal pollution in the marine environment (Mahboob et al., 2014Mahboob, S., Al-Balawi, H. F. A., Al-Misned, F., Al-Quraishy, S., & Ahmad, Z. (2014). Tissue metal distribution and risk assessment for important fish species from Saudi Arabia. Bulletin of Environmental Contamination and Toxicology, 92(1), 61-66. http://dx.doi.org/10.1007/s00128-013-1139-8. PMid:24201710.
http://dx.doi.org/10.1007/s00128-013-113...
; Freije, 2015Freije, A. M. (2015). Heavy metal, trace element and petroleum hydrocarbon pollution in the Arabian Gulf. Journal of the Association of Arab Universities for Basic and Applied Science, 17(1), 90-100. http://dx.doi.org/10.1016/j.jaubas.2014.02.001.
http://dx.doi.org/10.1016/j.jaubas.2014....
). In the Red Sea coastal area of Saudi Arabia, the increase in developmental activities, gold mining, and industrialization activities are the main reasons for heavy metal contamination of seafood products (Alnashiri, 2022Alnashiri, H. M. (2022). A brief review on heavy metal bioaccumulation studies from Red Sea. Adsorption Science and Technology, 2022, 6201299. http://dx.doi.org/10.1155/2022/6201299.
http://dx.doi.org/10.1155/2022/6201299...
). In recent decades, heavy metal contamination of fish and seafood has been of serious global concern, especially among consumers, health professionals, and seafood traders.

Fishes are important sources of high-quality protein and fat, and consequently, the consumption of these seafood products rapidly increased in recent years (Younis et al., 2021Younis, E. M., Abdel-Warith, A.-W. A., Al-Asgah, N. A., Elthebite, S. A., & Rahman, M. (2021). Nutritional value and bioaccumulation of heavy metals in muscle tissues of five commercially important marine fish species from the Red Sea. Saudi Journal of Biological Sciences, 28(3), 1860-1866. http://dx.doi.org/10.1016/j.sjbs.2020.12.038. PMid:33732073.
http://dx.doi.org/10.1016/j.sjbs.2020.12...
). However, they can be contaminated with various types of toxic heavy metals through the uptake and accumulation of these hazardous metals in muscles, and the concentration of such heavy metals in the fish muscles is regulated by the uptake and discharge mechanisms (Mansour & Sidky, 2002Mansour, S. A., & Sidky, M. M. (2002). Ecotoxicological studies. 3. Heavy metals contaminating water and fish from Fyoum Governorate, Egypt. Food Chemistry, 78(1), 15-22. http://dx.doi.org/10.1016/S0308-8146(01)00197-2.
http://dx.doi.org/10.1016/S0308-8146(01)...
). In addition, the distribution and accumulation levels of heavy metals in fish muscles depend on various factors such as fish type, age, season, and other physiological parameters (Bervoets et al., 2001Bervoets, L., Blust, R., & Verheyen, R. (2001). Accumulation of metals in the tissues of three spined stickleback (Gasterosteusaculeatus) from natural freshwater. Ecotoxicology and Environmental Safety, 48(2), 117-127. http://dx.doi.org/10.1006/eesa.2000.2010. PMid:11161686.
http://dx.doi.org/10.1006/eesa.2000.2010...
; Mansour & Sidky, 2002Mansour, S. A., & Sidky, M. M. (2002). Ecotoxicological studies. 3. Heavy metals contaminating water and fish from Fyoum Governorate, Egypt. Food Chemistry, 78(1), 15-22. http://dx.doi.org/10.1016/S0308-8146(01)00197-2.
http://dx.doi.org/10.1016/S0308-8146(01)...
). It has also been reported that heavy metals are taken up and cumulated in different fish organs at different levels. However, such accumulation is recorded to peak in the summer season, followed by autumn, winter, and spring seasons (Bervoets et al., 2001Bervoets, L., Blust, R., & Verheyen, R. (2001). Accumulation of metals in the tissues of three spined stickleback (Gasterosteusaculeatus) from natural freshwater. Ecotoxicology and Environmental Safety, 48(2), 117-127. http://dx.doi.org/10.1006/eesa.2000.2010. PMid:11161686.
http://dx.doi.org/10.1006/eesa.2000.2010...
; Mansour & Sidky, 2002Mansour, S. A., & Sidky, M. M. (2002). Ecotoxicological studies. 3. Heavy metals contaminating water and fish from Fyoum Governorate, Egypt. Food Chemistry, 78(1), 15-22. http://dx.doi.org/10.1016/S0308-8146(01)00197-2.
http://dx.doi.org/10.1016/S0308-8146(01)...
).

Based on heavy metals' importance and physiological roles, they are classified into different groups. Iron, cobalt, and zinc are classified as essential, nickel is classified as probably essential, and cadmium (Cd), lead (Pb), and mercury (Hg) are classified as toxic by intentional organizations such as the United States Environmental Protection Agency and World Health Organization (Micheline et al., 2019Micheline, G., Rachida, C., Céline, M., Gaby, K., Rachid, A., & Petru, J. (2019). Levels of Pb, Cd, Hg and As in fishery products from the eastern Mediterranean and human health risk assessment due to their consumption. International Journal of Environmental of Research, 13(3), 443-455. http://dx.doi.org/10.1007/s41742-019-00185-w.
http://dx.doi.org/10.1007/s41742-019-001...
). The consumption of heavy metals at low or high concentrations could be of high hazard depending on their classes. Consumption of low concentrations of toxic heavy metals (Cd, Pb, and Hg) over a long period can be very dangerous to humans due to the high toxicity of these elements. In addition, consuming high levels of essential heavy metals may also be toxic to humans (Celik & Oehlenschlager, 2004Celik, U., & Oehlenschlager, J. (2004). Determination of zinc and copper in fish samples collected from northeast Atlantic by DPSAV. Food Chemistry, 87(3), 343-347. http://dx.doi.org/10.1016/j.foodchem.2003.11.018.
http://dx.doi.org/10.1016/j.foodchem.200...
). The toxicity of heavy metals is due to the effect of such metals on cellular membranes, vital organelles, and biochemical processes driving enzymes as well as their contribution to the development of reactive oxygen species (Mahurpawar, 2015Mahurpawar, M. (2015). Effects of heavy metals on human health. International Journal of Research-GRANTHAALAYAH, 3(Spe 9), 1-7. http://dx.doi.org/10.29121/granthaalayah.v3.i9SE.2015.3282.
http://dx.doi.org/10.29121/granthaalayah...
). Therefore, consuming toxic heavy metals at doses > the recommended limits could affect the whole body's function and lead to death (Zaynab et al., 2022Zaynab, M., Al-Yahyai, R., Ameen, A., Sharif, Y., Ali, L., Fatima, M., Khan, K. A., & Li, S. (2022). Health and environmental effects of heavy metals. Journal of King Saud University-Science, 34(1), 101653. http://dx.doi.org/10.1016/j.jksus.2021.101653.
http://dx.doi.org/10.1016/j.jksus.2021.1...
).

Despite the specific toxicity reaction signs of individual heavy metals, the general signs of poisoning with aluminum, arsenic, cadmium, cancers, copper, lead, mercury, and zinc are ataxia, causing a rust-red colored stool, convulsions, depression, diarrhea, gastrointestinal disorders, hemoglobinuria, kidney failure, neurological diseases, paralysis, pneumonia, stomatitis, tremors, and vomiting (Alissa & Ferns, 2011Alissa, E. M., & Ferns, G. A. (2011). Heavy metal poisoning and cardiovascular disease. Journal of Toxicology, 2011, 870125. http://dx.doi.org/10.1155/2011/870125. PMid:21912545.
http://dx.doi.org/10.1155/2011/870125...
). In addition, heavy metals possess cytotoxicity, mutagenic, and carcinogenic properties, are resistant to degradation in the animal cells, accumulate in the animal tissues in excess amounts, and consequently affect human health (More et al., 2003More, T. G., Rajput, R. A., & Bandela, N. N. (2003). Impact of heavy metals on DNA content in the whole body of freshwater bivalve, Lamelleiden marginalis. Environmental Pollution and Research, 22, 605-616.).

Due to increased heavy metal pollution in the marine environment, investigating the levels of heavy metals in fish and seafood products is very important from the standpoints of health professionals, consumers, and traders. In Saudi Arabia, trading fishery products are not regulated by standard limits of heavy metals in these important products (Aljabryn, 2013Aljabryn, D. H. (2013). Monitoring trace metals in some cultured freshwater fish species in Saudi Arabia. Journal of Food Science and Engineering, 3, 481-488.). Therefore, this study focused on the levels of some heavy metals in some major, commercially important marine fisheries species belonging to three main categories, crustaceans, shellfish, and fish market in Jeddah is the main local fish market in Saudi Arabia. In addition, the possible seasonal impact on the acquisition of heavy metals by different examined species and the public health importance of the detected levels of heavy metals are also discussed.

2 Materials and methods

2.1 Materials

Fisheries samples

Three major and commercially important marine fisheries categories belong to crustaceans species, Fenneropenaeus indicus, shellfish species, Chaceon quinquedens and five fish species, Lethrinus nebulosus, Scomberomorus commerson, Plectropomus pessuliferus, Pampus argenteus and Epinephelus summana marketed in Jeddah main fish market, Saudi Arabia, were used in this study. All collected samples (n = 20 of each type) were of the same marketing size and seasons (winter, summer, and fall) during the year 2012 (Table 1). After collection, the samples were kept in an icebox and then transferred under cold conditions to the laboratory at Jeddah Fisheries Research Center. They were kept in a deep freezer at -20 ˚C for further analysis.

Table 1
List of examined fisheries species.

Chemicals and glassware

The chemical used in this study were of high chemical grades and were obtained from Sigma Aldrich (Sigma, MO, USA), JB Baker Inc. (Phillipsburg, NJ, USA), or BDH chemicals (Poole, England). All glassware were thoroughly washed with detergent, ddH2O water, and nitric acid and then dried in an oven (overnight at 130 ˚C) before use for sample preparation and analysis.

2.2 Methods

Sample preparation

Before the analysis of heavy metals, the muscle slices of individual fishery samples were subjected to dry ashing using a muffle furnace (Heraeus, Germany) at 550 °C for 6 h, following the method described by Crosby (1977)Crosby, N. T. (1977). Determination of metals in foods. Analyst, 102(1213), 225-268. http://dx.doi.org/10.1039/an9770200225. PMid:327849.
http://dx.doi.org/10.1039/an9770200225...
. After that, the ash was digested with concentrated nitric acid on a sand bath and then subjected to filtration through ash-less filter paper. The clear filtrate was used for the analysis of minerals using an atomic absorption spectrometer (AA-6200, Shimadzu, Kyoto, Japan).

Mineral analysis

The sample filtrates were analyzed for heavy metal content using an atomic absorption spectrometer as described in the instruction manual. The levels of the following trace elements: cadmium (Cd), chromium (Cr), cobalt (Co), copper (Cu), iron (Fe), lead (Pb), nickel (Ni), and zinc (Zn) in fishery samples were analyzed and considered as indicators of heavy metal pollution. The concentration of the aforementioned elements was determined on the dry weight base.

2.3 Statistical analysis

Triplicate samples of each fishery product were analyzed, and the results were subjected to statistical analysis using the Statistical Package of Costas Program (CoStat, 1986CoStat. (1986). Version 2. Minneapolis: Cohort Software.). The results were subjected to analysis of variance (ANOVA) and were presented as the means ± standard deviations (SD). The significance was accepted at the probability of 0.05 or less (P ≤ 0.05).

3 Results and discussion

This study highlights heavy metals contents in some major and commercially important marine fisheries species belonging to crustaceans, shellfish, and fish categories in Jeddah are main local fish market, Saudi Arabia, throughout the winter, summer, and fall seasons of the year 2012 (Tables 2-4) respectively.

Table 2
Levels of heavy metals in marine fish species (mg/kg fresh weight) in winter season 2012.
Table 4
Levels of heavy metals in marine fish species (mg/kg fresh weight) in fall season 2012.

Regarding As residues, the highest recorded levels were in C. quinquedens, with estimated mean values ranging from 3.63 ± 0.09 (Table 4) to 4.30 ± 0.10 mg/kg (Table 2), followed by in F. indicus the mean detected levels ranged from 0.59 ± 0.01 (Table 2) to 0.70 ± 0.03 mg/kg (Table 4). Though, the mean estimated levels of As in L. nebulosus, P. pessuliferus, E. summana, P. argenteus and S. commerson ranged from 0.23 ± 0.02 (Table 2) to 0.26 ± 0.01 (Table 3); 0.21 ± 0.05 (Table 3) to 0.26 ± 0.02 (Table 4); 0.21 ± 0.01(Table 2) to 0.23 ± 0.04 (Table 4); 0.14 ± 0.06 (Table 4) to 0.19 ± 0.02 (Table 2) and 0.16 ± 0.03 (Table 3) to 0.18 ± 0.01 mg/kg (Table 2) respectively. The statistical analysis results revealed high significant differences were shown in As levels between C. Quinquedens and all other species at p ≤ 0.05 level, followed by F. indicus, while no significant differences have appeared between the other species‎ at the same level. Also, no significant differences appeared in As levels in the same species of all studied marine fish species in the different seasons at P ≤ 0.05 level.

Table 3
Levels of heavy metals in marine fish species (mg/kg fresh weight) in summer season 2012.

Compared to the standard permissible limits of 0.5, 0.5, and 0.2 mg/kg for shellfish, crustaceans, and marine fishes, respectively (Saudi Arabia Standards Organization, 1997Saudi Arabia Standards Organization – SASO. (1997). Maximum limits of contaminating metallic elements in foods. Riyadh: SASO.), C. quinquedens, F. indicus, L. nebulosus, P. pessuliferus, and E. summana exceeded the permissible standards, however, P. argenteus and S. commerson are considered border lines. In this sense, Hall et al. (1978)Hall, R. A., Zook, E. G., & Meaburn, G. M. (1978). National marine fisheries service survey of trace elements in the fishery resource. Washington, D.C.: U.S. Department of Commerce/National Oceanic and Atmospheric Administration/National Marine Fisheries Service. stated that the inorganic form of As, the dangerous component, constitutes about 10% of the total As. However, 85% - 95% of the total As is the form of the non-dangerous organic component. In this regard, the United States Food and Drug Administration (Food and Drug Administration, 1993aFood and Drug Administration – FDA. (1993a). Guidance document for chromium in shellfish. Washington, D.C.: DHHS/PHS/FDA/CFSAN/Office of Seafood.) recorded that As levels in clams, oysters, crabs, and crustaceans reached (0.82-6.6 mg/kg), (1.4-2.8 mg/kg), (10-30 mg/kg) and (8.6-10.6 mg/kg), respectively In winter season, the level of Co was higher significantly in P. argenteus in compare with the other species, followed by S. commerson and then L. nebulosus, and in the other species were in the 4th order with no significant differences were appeared between ‎ it at p ≤ 0.05‎ level.

P. pessuliferu showed a significant difference (at p ≤ 0.05‎) in Ni concentration compared with the other species in winter, followed by L. nebulosus, S. commerson, P. argenteus, and E. summana has come at last. The Zn level in P. pessuliferu increased significantly at p ≤ 0.05 level. Followed by both L. nebulosus and E. summana, then both P. pessuliferus C. quinquedens, and finally F. indicus. Statistically, Fe quantities in the winter season were varied with significant differences among E. summana and L. nebulosus and P. argenteus and S. commerson, and both C. quinquedens and P. pessuliferus respectively at P ≤ 0.05 level. Significant differences have appeared in Cr levels in marine fish species in the winter season between S. commerson and all other species, followed by L. nebulosus and E. summana, while all other species came at the 3rd order with no significant differences among it at P ≤ 0.05 level.

The results in Table 3 reveal that, in summer season, As the level in F. indicus recorded high significant differences in comparison with all other marine fish species at level P ≤ 0.05. Also, F. indicus in addition to C. quinquedens were surpassed all other species in Co levels at level P ≤ 0.05‎. The results showed significant differences in Zn between both of E. summana and P. pessuliferus, and both of L. nebulosus and P. argenteus, and then C. quinquedens, F. indicus, S. commerson respectively at P ≤ 0.05 level.

‎The levels of Fe have differed significantly between the studied marine fish samples in ‎the summer level at level P ≤ 0.05 in the following order, L. nebulosus, P. argenteus, each ‎of (F. indicus E. summana, C. quinquedens), P. pessuliferus and S. commerson ‎respectively. Also, there are significant differences in the Cr level between F. indicus and C. quinquedens at level P ≤ 0.05‎.

In the fall season, the results in Table 4 reveal that the level of As in ‎C. quinquedens‎ increased with high significant differences compared with all other marine fish species at level P ≤ 0.05. Likewise, C. quinquedens in addition to F. indicus and P. argenteus were exceeded all other species in Co levels, followed by both S. commerson and L. nebulosus, and finally E. summana at level P ≤ 0.05‎. The results of Ni levels showed significant differences between both S. commerson and L. nebulosus compared with all other marine fish species at level P ≤ 0.05. There are significant differences in the Zn level in the fall season between E. summana and L. nebulosus followed by (P. argenteus, P. pessuliferus, C. quinquedens), both S. commerson ‎and F. indicus at level P ≤ 0.05. The results also reveal that the level of Cr in ‎ F. indicus‎ increased with highly significant differences compared with all other marine fish species at level P ≤ 0.05.

Data shown in Table 2 revealed that Pb residues were only detected in the winter season in P. pessuliferus, E. summana, P. argenteus, L. nebulosus and S. commerson, with mean levels of 5.05 ± 0.86; 2.80 ± 0.35; 1.69 ± 0.04; 1.51 ± 0.06 and 0.89 ± 0.14 mg/kg, respectively, as indicated in Table 2, the levels of Pb were varied with significant differences between at p ≤ 0.05, suggesting the possible impact of low water temperature during the winter season on the acquisition mechanism of Pb by marine fish species. However, it appeared also that seasonal impacts might play a role in the absence of Pb from all other examined marine fisheries species in the summer and fall seasons (Tables 3-4), respectively. Comparatively, the recorded Pb levels are greater than the maximum permissible recorded limit of 0.5 mg/kg for Saudi Arabian marine fisheries species (Saudi Arabia Standards Organization, 1997Saudi Arabia Standards Organization – SASO. (1997). Maximum limits of contaminating metallic elements in foods. Riyadh: SASO.). The absence of Pb from F. indicus and C. quinquedens could be attributed to the significant role of feeding habits of these crustaceans and shellfish species as bottom feeders compared to other tested fish species. However, the slightly greater levels of Pb in all fish samples might result from manufacturing and/or natural geochemical activities, the matter that may also reflect the existence of pollution in the marine environment (Belitz et al., 2004Belitz, H. D., Grosch, W., & Schieberle, P. (2004). Food chemistry. Berlin: Springer. http://dx.doi.org/10.1007/978-3-662-07279-0.
http://dx.doi.org/10.1007/978-3-662-0727...
; Carvalho et al., 2005Carvalho, M. L., Santiago, S., & Nunes, M. L. (2005). Assessment of the essential element and heavy metal content of edible fish muscle. Analytical and Bioanalytical Chemistry, 382(2), 426-432. http://dx.doi.org/10.1007/s00216-004-3005-3. PMid:15830192.
http://dx.doi.org/10.1007/s00216-004-300...
).

In contrast, Pb contents were recorded in ranges of 0.09-6.95, 0.22-0.85, and 0.07-0.87 mg/kg in fish species from Iskenderun Bay (Türkmen et al., 2005Türkmen, A., Türkmen, M., Tepe, Y., & Akyurt, İ. (2005). Heavy metals in three commercially valuable fish species from İskenderun Bay, northern east Mediterranean Sea, Turkey. Food Chemistry, 91(1), 167-172. http://dx.doi.org/10.1016/j.foodchem.2004.08.008.
http://dx.doi.org/10.1016/j.foodchem.200...
), fish from the Black Sea (Tüzen, 2003Tüzen, M. (2003). Determination of heavy metals in fish samples of the middle Black Sea (Turkey) by graphite furnace atomic absorption spectrometry. Food Chemistry, 80(1), 119-123. http://dx.doi.org/10.1016/S0308-8146(02)00264-9.
http://dx.doi.org/10.1016/S0308-8146(02)...
) and Turkish Northeast Atlantic fish (Yılmaz et al., 2007Yılmaz, F., Özdemir, N., Demirak, A., & Tuna, A. L. (2007). Heavy metals levels in two fish species Leuciscuscephalus and Lepomisgibbosus. Food Chemistry, 100(2), 830-835. http://dx.doi.org/10.1016/j.foodchem.2005.09.020.
http://dx.doi.org/10.1016/j.foodchem.200...
) respectively. However, a Pb level of 0.5 mg/kg was reported as the maximum permissible limit in marine fishes (Nauen, 1983Nauen, C. E. (1983). Compilation of legal limits for hazardous substances in fish and fishery products. Rome: FAO Fisheries Circular.). Lead is known as one of the most hazardous heavy metals. It causes an elevation in hypertension and promotion of cardiovascular disease in adults and reduces intellectual activities in children (Commission of the European Communities, 2006Commission of the European Communities. (2006, December 19). Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Union, L 364.). Therefore, contamination of fishery products with this heavy metal is of great concern from the standpoints of health workers and fishery product consumers.

The mean estimated levels of Co in the winter season ranged from 2.17 ± 0.04 to 7.74 ± 0.45 mg/kg in C. quinquedens and P. argenteus, respectively Table 2. However, the mean levels in the summer season Table 3 were in the range of 0.26 ± 0.05 to 2.32 ± 0.07 mg/kg in E. summana and C. quinquedens, respectively. On the other hand, Table 4 showed that Co mean levels in the fall season were within the range of 0.41 ± 0.28 to 2.38 ± 0.28 mg/kg in P. pessuliferus and P. argenteus, respectively.

Statistically, significant differences have appeared in Co levels of E. summana, P. pessuliferus between winter and summer and fall seasons at P ≤ 0.05 level. For P. argenteus, S. commerson, and L. nebulosus, Co levels significantly differed in winter, followed by the fall and summer seasons, respectively. Also, no significant differences were shown in the Co levels in both F. indicus and C. quinquedens between the seasons.

Similar to our findings, Similar to our findings, Co was reported to be at high and moderate levels in Oreochromis niloticus, Clarias lazera, and Cyprinus carpio from freshwater fish farm in Al-Kharj, Saudi Arabia (Aljabryn, 2013Aljabryn, D. H. (2013). Monitoring trace metals in some cultured freshwater fish species in Saudi Arabia. Journal of Food Science and Engineering, 3, 481-488.). In addition, high levels of Co were also reported in the muscles of Euryglossa orientalis (3.21 mg/kg) and Otolithes ruber (1.94 mg/kg) from Arvand River, Iran (Sheikhzadeh & Hamidian, 2021Sheikhzadeh, H., & Hamidian, A. H. (2021). Bioaccumulation of heavy metals in fish species of Iran: a review. Environmental Geochemistry and Health, 43(10), 3749-3869. http://dx.doi.org/10.1007/s10653-021-00883-5. PMid:33818681.
http://dx.doi.org/10.1007/s10653-021-008...
). On the other hand, Co was not detected in the fish samples obtained from Ataturk Dam Lake, Turkey (Karadede et al., 2004Karadede, H., Oymak, S. A., & Unlu, E. (2004). Heavy metals in mullet, Liza abu and catfish, Silurustriostegus from the Ataturk Dam Lake (Euphrates), Turkey. Environment International, 30(2), 183-188. http://dx.doi.org/10.1016/S0160-4120(03)00169-7. PMid:14749107.
http://dx.doi.org/10.1016/S0160-4120(03)...
). The variations among these studies are likely due to the differences in the fish species, collection location and season, and environmental conditions. Being a part of vitamin B12, Co represents one of the essential heavy metals with high health benefits, which acts as a regulator of blood pressure and is vital for the thyroid gland's proper functioning. However, excessive intake and accumulation of Co in the human body may cause congestive heart failure, anemia, polycythemia, overproduction of erythrocytes, and pulmonary fibrosis (Sheikhzadeh & Hamidian, 2021Sheikhzadeh, H., & Hamidian, A. H. (2021). Bioaccumulation of heavy metals in fish species of Iran: a review. Environmental Geochemistry and Health, 43(10), 3749-3869. http://dx.doi.org/10.1007/s10653-021-00883-5. PMid:33818681.
http://dx.doi.org/10.1007/s10653-021-008...
).

The mean estimated levels of Ni in the winter season in Table 2 revealed ranged from non-detection in F. indicus & C. quinquedens to 5.70 ± 0.28 mg/kg in P. pessuliferus. Meanwhile, Ni was not detected in all examined species in the summer season (Table 3). However, in the fall season (Table 4), Ni means estimated values ranged from non-detection in F. indicus & C. quinquedens to 3.80 ± 0.10 mg/kg in L. nebulosus, suggesting the possible seasonal impact and feeding habitat on the acquisition of Ni by the examined species. The levels of Ni in E. summana and P. argenteus, S. commerson, and L. nebulosus were significantly higher in fall compared with winterseason, while in P. pessuliferus it was significantly higher in winter compared with fall season at P ≤ 0.05 level. Previously, high levels of Ni were detected in the liver (286.4 mg/kg wet weight basis) and muscle (11.46 mg/kg wet weight basis) tissues of Johnius belangerii from Khark Island and Musa Estuary, Iran, respectively (Sheikhzadeh & Hamidian, 2021Sheikhzadeh, H., & Hamidian, A. H. (2021). Bioaccumulation of heavy metals in fish species of Iran: a review. Environmental Geochemistry and Health, 43(10), 3749-3869. http://dx.doi.org/10.1007/s10653-021-00883-5. PMid:33818681.
http://dx.doi.org/10.1007/s10653-021-008...
). In addition, high levels (6.33-10.74 mg/kg DW) of Ni were also reported in muscles of Clarias lazera, while moderate levels (3.42-4.15 mg/kg DW) were found Cyprinus carpio and Oreochromis niloticus from a freshwater fish farm in Al-Kharj, Saudi Arabia (Aljabryn, 2013Aljabryn, D. H. (2013). Monitoring trace metals in some cultured freshwater fish species in Saudi Arabia. Journal of Food Science and Engineering, 3, 481-488.). In other studies for Turkey, Ni ranges of 0.11-12.90 mg/kg DW and 0.93-2.77 mg/kg DW were reported for fish species from Iskenderun Bay and Dhanmondi Lake, respectively (Türkmen et al., 2005Türkmen, A., Türkmen, M., Tepe, Y., & Akyurt, İ. (2005). Heavy metals in three commercially valuable fish species from İskenderun Bay, northern east Mediterranean Sea, Turkey. Food Chemistry, 91(1), 167-172. http://dx.doi.org/10.1016/j.foodchem.2004.08.008.
http://dx.doi.org/10.1016/j.foodchem.200...
; Begum et al., 2005Begum, A., Amin, M. N., Kaneco, S., & Ohta, K. (2005). Selected elemental composition of the muscle tissue of three species of fish, Tilapia nilotica, Cirrhinamrigola and Clariasbatracus, from the freshwater Dhanmondi lake in Bangladesh. Food Chemistry, 93(3), 439-443. http://dx.doi.org/10.1016/j.foodchem.2004.10.021.
http://dx.doi.org/10.1016/j.foodchem.200...
). Moreover, low levels (0.42-0.85 mg/kg DW) of Ni were detected in canned fish from Bangladesh (Tuzen & Soylak, 2006Tuzen, M., & Soylak, M. (2006). Chromium speciation in environmental samples by solid phase extraction on Chromosorb 108. Journal of Hazard Materials, 129(1-3), 266-273. http://dx.doi.org/10.1016/j.jhazmat.2005.08.046. PMid:16236441.
http://dx.doi.org/10.1016/j.jhazmat.2005...
). The variation in Ni content among these studies could be due to the variations in the fish species, catching season and location, handling and processing methods, and environmental conditions. Despite the lack of data about Saudi Arabian permissible Ni contents in fish, the Ni values of this study are within the acceptable range based on the FDA regulations that set the allowable level of Ni as 70-80 mg/kg (Food and Drug Administration, 1993bFood and Drug Administration – FDA. (1993b). Guidance document for nickel in shellfish. Washington, D.C.: DHHS/PHS/FDA/CFSAN/Office of Seafood.). Although Ni and Cr are dangerous metals and maximum allowable limits were set by FDA, the European Union (EC) did not make any regulations about these trace elements in fish and other aquatic products (Aljabryn, 2013Aljabryn, D. H. (2013). Monitoring trace metals in some cultured freshwater fish species in Saudi Arabia. Journal of Food Science and Engineering, 3, 481-488.).

The mean estimated values of Cu in the winter season Table 2 ranged from non-detection in F. indicus, C. quinquedens, L. nebulosus, and S. commerson to 1.18 ± 1.08 mg/kg in E. summana. However, data shown in Table 3 revealed that the mean levels of Cu in the summer season ranged from non-detection in F. indicus, C. quinquedens, L. nebulosus, and P. argenteus to 0.11 ± 0.07 mg/kg in P. pessuliferus. Meanwhile, Cu was only detected in S. commerson and E. summana samples during the fall season (Table 4), with mean values of 0.41 ± 0.22 and 0.48 ± 0.42 mg/kg, respectively. The Cu contents of E. summana and S. commerson were significantly increased in fall season compared to that in winter season at P ≤ 0.05 level, while in P. pessuliferus it was was significantly higher in summer compared with winter season at P ≤ 0.05 level, and in E. summana Cu was increased with significant differences in winter compared to fall season in the same level.

However, the recorded Cu levels were lower than the maximum allowable limit of 20 mg/kg reported by Centre for Environment, Fisheries and Aquaculture Science (1995)Centre for Environment, Fisheries and Aquaculture Science – Cefas. (1995). Monitoring and surveillance of non-radioactive contaminants in the aquatic environment and activities of regulating the disposal of wastes at Sea (1993). Lowestoft: Cefas. Aquatic Environment Monitoring Report No. 44.. Copper is an important trace element with various roles in metabolisms and hemoglobin synthesis because it is the main component of the same important enzymes (Sheikhzadeh & Hamidian, 2021Sheikhzadeh, H., & Hamidian, A. H. (2021). Bioaccumulation of heavy metals in fish species of Iran: a review. Environmental Geochemistry and Health, 43(10), 3749-3869. http://dx.doi.org/10.1007/s10653-021-00883-5. PMid:33818681.
http://dx.doi.org/10.1007/s10653-021-008...
). However, the consumption of excess amounts of copper, which is found in high concentrations in seafood, has high health concerns as it may cause damage to the kidney and liver (Yap et al., 2016Yap, C. K., Cheng, W. H., Karami, A., & Ismail, A. (2016). Health risk assessments of heavy metal exposure via consumption of marine mussels collected from anthropogenic sites. The Science of the Total Environment, 553, 285-296. http://dx.doi.org/10.1016/j.scitotenv.2016.02.092. PMid:26925739.
http://dx.doi.org/10.1016/j.scitotenv.20...
).

The mean estimated values of Zn in the winter season (Table 2) ranged from 1.94 ± 0.78 to 6.29 ± 0.26 mg/kg in F. indicus and S. commerson, respectively. However, in the summer season (Table 3), the mean values of Zn were in the range of 0.99 ± 0.02 to 5.40 ± 0.66 mg/kg in S. commerson and E. summana, respectively. Meanwhile, Zn mean levels in the fall season (Table 4) ranged from 1.81 ± 0.08 to 5.91 ± 0.25 mg/kg in F. indicus and E. summana, respectively.

The contents of Zn were high with significant differences in S. commerson in winter compared with fall and summer seasons. Also, it was high with significant differences P. pessuliferus and F. indicus summer followed by winter and fall seasons respectively, and in P. argenteus it was higher in summer followed by fall and winter seasons respectively, while in E. summana it was lowered in winter compared to both summer and fall seasons at P ≤ 0.05 level.

A previous study has shown high levels (16.79-49.43 mg/kg DW) of Zn in fish species (blackspot, emperors, grouper, and sardines) obtained from different districts in Saudi Arabia (Alturiqi & Albedair, 2012Alturiqi, A. S., & Albedair, L. A. (2012). Evaluation of some heavy metals in certain fish, meat and meat products in Saudi Arabian markets. Egyptian Journal of Aquatic Research, 38(1), 45-49. http://dx.doi.org/10.1016/j.ejar.2012.08.003.
http://dx.doi.org/10.1016/j.ejar.2012.08...
). In addition, comparable levels (1.48-11.9 mg/kg DW) of Zn were found in three fish species obtained from fish farms in the Al-Kharj area, Saudi Arabia (Aljabryn, 2013Aljabryn, D. H. (2013). Monitoring trace metals in some cultured freshwater fish species in Saudi Arabia. Journal of Food Science and Engineering, 3, 481-488.). Moreover, varied levels of Zn were reported in fish species from Iskenderun Bay (0.60-11.60 mg/kg DW) and Black Sea (9.50-22.90 mg/kg DW) in Turkey (Tüzen, 2003Tüzen, M. (2003). Determination of heavy metals in fish samples of the middle Black Sea (Turkey) by graphite furnace atomic absorption spectrometry. Food Chemistry, 80(1), 119-123. http://dx.doi.org/10.1016/S0308-8146(02)00264-9.
http://dx.doi.org/10.1016/S0308-8146(02)...
; Türkmen et al., 2005Türkmen, A., Türkmen, M., Tepe, Y., & Akyurt, İ. (2005). Heavy metals in three commercially valuable fish species from İskenderun Bay, northern east Mediterranean Sea, Turkey. Food Chemistry, 91(1), 167-172. http://dx.doi.org/10.1016/j.foodchem.2004.08.008.
http://dx.doi.org/10.1016/j.foodchem.200...
), while Celik & Oehlenschlager (2004)Celik, U., & Oehlenschlager, J. (2004). Determination of zinc and copper in fish samples collected from northeast Atlantic by DPSAV. Food Chemistry, 87(3), 343-347. http://dx.doi.org/10.1016/j.foodchem.2003.11.018.
http://dx.doi.org/10.1016/j.foodchem.200...
recorded Zn range of 2.1-8.7 mg/kg in North-East Atlantic fish. However, our recorded levels of Zn are the lowest compared to the standard permissible limits of 50.00 and 30.00 mg/kg recorded by Centre for Environment, Fisheries and Aquaculture Science (1995)Centre for Environment, Fisheries and Aquaculture Science – Cefas. (1995). Monitoring and surveillance of non-radioactive contaminants in the aquatic environment and activities of regulating the disposal of wastes at Sea (1993). Lowestoft: Cefas. Aquatic Environment Monitoring Report No. 44. and Nauen (1983)Nauen, C. E. (1983). Compilation of legal limits for hazardous substances in fish and fishery products. Rome: FAO Fisheries Circular., respectively. The differences in Zn content among the aforementioned studies are probably due to the variations in the fish genotypes, age, season, location, and environmental conditions. From a health point of view, Zn has an important role in human health as it involves various enzymatic activities and metabolic processes to maintain the structural integrity of proteins, maintains the system functions, and possesses antioxidant and anti-inflammation properties (Izah et al., 2017Izah, S. C., Inyang, I. R., Angaye, T. C., & Okowa, I. P. (2017). A review of heavy metal concentration and potential health implications of beverages consumed in Nigeria. Toxics, 5(1), 1. http://dx.doi.org/10.3390/toxics5010001. PMid:29051433.
http://dx.doi.org/10.3390/toxics5010001...
; Choi et al., 2018Choi, S., Liu, X., & Pan, Z. (2018). Zinc deficiency and cellular oxidative stress: prognostic implications in cardiovascular diseases. Acta Pharmacologica Sinica, 39(7), 1120-1132. http://dx.doi.org/10.1038/aps.2018.25. PMid:29926844.
http://dx.doi.org/10.1038/aps.2018.25...
). The deficiency of Zn is linked to growth retardation, taste loss, anemia, decreased fertility, and cardiovascular diseases (Choi et al., 2018Choi, S., Liu, X., & Pan, Z. (2018). Zinc deficiency and cellular oxidative stress: prognostic implications in cardiovascular diseases. Acta Pharmacologica Sinica, 39(7), 1120-1132. http://dx.doi.org/10.1038/aps.2018.25. PMid:29926844.
http://dx.doi.org/10.1038/aps.2018.25...
). However, the consumption of excess amounts of Zn is toxic to the human body and organs (Yap et al., 2016Yap, C. K., Cheng, W. H., Karami, A., & Ismail, A. (2016). Health risk assessments of heavy metal exposure via consumption of marine mussels collected from anthropogenic sites. The Science of the Total Environment, 553, 285-296. http://dx.doi.org/10.1016/j.scitotenv.2016.02.092. PMid:26925739.
http://dx.doi.org/10.1016/j.scitotenv.20...
).

The mean estimated values of Fe in tested species in the winter season (Table 2) ranged from 3.50 ± 0.27 to 9.09 ± 0.89 mg/kg in P. pessuliferus and E. summana, respectively. However, in the summer season (Table 3), the mean values of Fe ranged from 2.65 ± 0.17 to 6.58 ± 0.11 mg/kg in S. commerson and L. nebulosus, respectively. The Fe was only noticed in the fall season (Table 4) in samples of F. indicus, C. quinquedens, and E. summana species with mean values of 3.88 ± 0.27, 3.57 ± 0.31, and 2.30 ± 0.07 mg/kg respectively. No significant differences were appeared in Fe levels in each of C. quinquedens, P. argenteus, and P. pessuliferus in the three seasons, however, in F. indicus it was significantly higher in both winter and summer compared to fall seasons, in E. summana and L. nebulosus it increased significantly in winter compared to the summer season at P ≤ 0.05 level.

Significantly high levels (81.60-188.60 mg/kg DW) of Fe were detected in fish species collected from Jeddah Coast, Red Sea, Saudi Arabia (Younis et al., 2021Younis, E. M., Abdel-Warith, A.-W. A., Al-Asgah, N. A., Elthebite, S. A., & Rahman, M. (2021). Nutritional value and bioaccumulation of heavy metals in muscle tissues of five commercially important marine fish species from the Red Sea. Saudi Journal of Biological Sciences, 28(3), 1860-1866. http://dx.doi.org/10.1016/j.sjbs.2020.12.038. PMid:33732073.
http://dx.doi.org/10.1016/j.sjbs.2020.12...
). In addition, the Fe content of farmed fishes from the Al-Kharj area, Saudi Arabia, ranged from 1.1-20.45 mg/kg DW (Aljabryn, 2013Aljabryn, D. H. (2013). Monitoring trace metals in some cultured freshwater fish species in Saudi Arabia. Journal of Food Science and Engineering, 3, 481-488.). Moreover, Fe of different fishes from the Caspian Sea, Iran, was in the wide range of 2.1-1343.5 mg/kg DW (Sheikhzadeh & Hamidian, 2021Sheikhzadeh, H., & Hamidian, A. H. (2021). Bioaccumulation of heavy metals in fish species of Iran: a review. Environmental Geochemistry and Health, 43(10), 3749-3869. http://dx.doi.org/10.1007/s10653-021-00883-5. PMid:33818681.
http://dx.doi.org/10.1007/s10653-021-008...
). The variations among these studies could be due to the differences in fish species, season, location, and environmental conditions. Data are missing regarding the acceptable standards of Fe in fisheries species in Saudi Arabia (Aljabryn, 2013Aljabryn, D. H. (2013). Monitoring trace metals in some cultured freshwater fish species in Saudi Arabia. Journal of Food Science and Engineering, 3, 481-488.). Fe is one of the most important essential heavy metals for the human body. It has significant roles in various physiological and biochemical pathways as a cofactor of some enzymes and the synthesis of blood cells (Abarshi et al., 2017Abarshi, M. M., Dantala, E. O., & Mada, S. B. (2017). Bioaccumulation of heavy metals in some tissues of croaker fish from oil spilled rivers of Niger Delta region, Nigeria. Asian Pacific Journal of Tropical Biomedicine, 7(6), 563-568. http://dx.doi.org/10.1016/j.apjtb.2017.05.008.
http://dx.doi.org/10.1016/j.apjtb.2017.0...
).

Cadmium was only detected in F. indicus and C. quinquedens with mean levels in winter, summer and fall seasons reached 0.23 ± 0.01 & 0.16 ± 0.02 (Table 2); 0.26 ± 0.01 & 0.21 ± 0.02 (Table 3) and 0.22 ± 0.01 & 0.19 ± 0.02 mg/kg (Table 4) respectively. No significant differences appeared in Cd levels in C. quinquedens in the three seasons, while it was increased significantly in F. indicus in both winter and summer compared to fall season at P ≤ 0.05 level.

These detected levels exceeded the permissible standard limits of 0.1 mg/kg recorded for Cd in Saudi Arabian crustaceans and shellfish (Saudi Arabia Standards Organization, 1997Saudi Arabia Standards Organization – SASO. (1997). Maximum limits of contaminating metallic elements in foods. Riyadh: SASO.). Meanwhile, Centre for Environment, Fisheries and Aquaculture Science (1995)Centre for Environment, Fisheries and Aquaculture Science – Cefas. (1995). Monitoring and surveillance of non-radioactive contaminants in the aquatic environment and activities of regulating the disposal of wastes at Sea (1993). Lowestoft: Cefas. Aquatic Environment Monitoring Report No. 44. reported a 2.0 mg/kg Cd permissible limit for fisheries products. The only detection of Cd in F. indicus and C. quinquedens may highlight the existence of environmental pollution. It may be explained on the bases of the existed differences in the acquisition mechanism of Cd by crustaceans and shellfish as bottom feeders in contrast to other examined marine fish species.

The estimated mean levels of Chromium in the winter season (Table 2) ranged from 1.70 ± 0.17 to 4.33 ± 0.28 mg/kg in P. pessuliferus and S. commerson, respectively. However, Data shown in (Table 3) revealed only detection of Cr in the summer season in F. indicus and C. quinquedens with mean values of 2.24 ± 0.14 and 1.74 ± 0.16 mg/kg, respectively. Meanwhile, in the fall season (Table 4), Cr was only detected in F. indicus, C. quinquedens, L. nebulosus, and P. argenteus samples with mean values of 1.95 ± 0.14, 1.51 ± 0.02, 0.18 ± 0.07 and 0.15 ± 0.08 mg/kg respectively. The level of Cr in C. quinquedens was high significantly in winter compared with both fall and summer seasons, where no significant differences were appeared in Cr levels in the two seasons, and in F. indicus it was higher with significant differences in both winter and summer compared to fall season, while in both L. nebulosus and P. argenteus it was higher significantly in winter compared to fall season at P ≤ 0.05 level.

These variations may reflect the seasonal impact and nutritional habitat on the acquisition of Cr by marine species. Our results are comparable to those documented for fish species obtained from Iskenderun Bay, Turkey (0.07-6.46 mg/kg DW) and in canned fish (0.97-1.70 mg/kg DW) as reported by Türkmen et al. (2005)Türkmen, A., Türkmen, M., Tepe, Y., & Akyurt, İ. (2005). Heavy metals in three commercially valuable fish species from İskenderun Bay, northern east Mediterranean Sea, Turkey. Food Chemistry, 91(1), 167-172. http://dx.doi.org/10.1016/j.foodchem.2004.08.008.
http://dx.doi.org/10.1016/j.foodchem.200...
and Tuzen & Soylak (2006)Tuzen, M., & Soylak, M. (2006). Chromium speciation in environmental samples by solid phase extraction on Chromosorb 108. Journal of Hazard Materials, 129(1-3), 266-273. http://dx.doi.org/10.1016/j.jhazmat.2005.08.046. PMid:16236441.
http://dx.doi.org/10.1016/j.jhazmat.2005...
, respectively. In the human body, Cr is involved in insulin function and lipid metabolism, however, excess Cr can cause damage to the liver, kidney, DNA, and nervous tissues (Yuan et al., 2020Yuan, Y., Sun, T., Wang, H., Liu, Y., Pan, Y., Xie, Y., Huang, H., & Fan, Z. (2020). Bioaccumulation and health risk assessment of heavy metals to bivalve species in Daya Bay (South China Sea): consumption advisory. Marine Pollution Bulletin, 150, 110717. http://dx.doi.org/10.1016/j.marpolbul.2019.110717. PMid:31753566.
http://dx.doi.org/10.1016/j.marpolbul.20...
).

The cumulative impacts of different amounts of heavy elements on the health status and vital body systems as well as their role as mediators of some human cancers, have been studied (Hertz-Picciotto, 2000Hertz-Picciotto, I. (2000). The evidence that lead increases the risk for spontaneous abortion. American Journal of Industrial Medicine, 38(3), 300-309. http://dx.doi.org/10.1002/1097-0274(200009)38:3<300::AID-AJIM9>3.0.CO;2-C. PMid:10940968.
http://dx.doi.org/10.1002/1097-0274(2000...
; Silbergeld et al., 2000Silbergeld, E. K., Waalkes, M., & Rice, J. M. (2000). Lead as a carcinogen: experimental evidence and mechanisms of actions. American Journal of Industrial Medicine, 38(3), 316-323. http://dx.doi.org/10.1002/1097-0274(200009)38:3<316::AID-AJIM11>3.0.CO;2-P. PMid:10940970.
http://dx.doi.org/10.1002/1097-0274(2000...
; Bal et al., 2000Bal, W., Kozlowski, H., & Kasprzak, K. S. (2000). Molecular models in nickel carcinogenesis. Journal of Inorganic Biochemistry, 79(1-4), 213-218. http://dx.doi.org/10.1016/S0162-0134(99)00169-5. PMid:10830868.
http://dx.doi.org/10.1016/S0162-0134(99)...
). However, additional research is required to highlight the acquisition mechanisms of these metal contaminants in different aquatic environments by crustaceans, fish, and shellfish species.

4 Conclusion

In conclusion, this study demonstrated that the mean values of most detected metals in seasonally examined marine fisheries species from Jeddah main fish market, Saudi Arabia, were within the standard allowable limits except for the recorded high mean values of As in F. indicus, C. quinquedens, L. nebulosus, P. pessuliferus, and E. summana compared to the standard permissible limits. In addition, Pb showed higher mean levels in S. commerson and P. pessuliferus compared to the standard permissible limits. However, Cd was not detected in all examined species, except for F. indicus and C. quinquedens where their levels exceeded the permissible standards. It appeared that seasonal impacts and species variations might play significant roles in the acquisition mechanisms of heavy metals in marine environments. Therefore, from a public health standpoint, applying a detection program for cumulative residual levels of heavy metals in marine fisheries species, especially crustaceans and shellfish, are recommended before marketing to ensure its safety.

Acknowledgements

This research was funded by Princess Nourah bint Abdulrahman University Researchers Supporting Project Number PNURSP2022R248, Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

  • Pratic Application: Control of fish contamination detection program for cumulative residual levels of heavy metals in marine fisheries products is recommended.
  • Availability of data and material

    The data used to support the findings of this study are included within the article.

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Publication Dates

  • Publication in this collection
    24 June 2022
  • Date of issue
    2022

History

  • Received
    12 Mar 2022
  • Accepted
    28 May 2022
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