3.1. Heavy Metal Concentrations in SeafoodAverage concentrations of nine heavy metals in edible tissues of fish, molluscs, and crustaceans collected from Pattani Bay in wet and dry seasons were shown in
Figure 2., The one-way ANOVA analysis showed significant variations of metal concentrations among species indicating that heavy metal accumulation differed in marine tissues. These variations were similar to those found in a previous study [
16]. The highest concentrations of most studied heavy metals, except for Cr, Cu, and Pb were found in molluscs and significantly greater than in fish and crustaceans. The greatest concentrations of metals found in molluscs were 0.78 mg Cd/kg ww (T. granosa), 0.75 mg Co/kg ww (M. meretrix), 227.72 mg Fe/kg ww (M. meretrix), 7.04 mg Mn/kg ww (P. erosa), 1.83 mg Ni/kg ww (P. erosa), and 198.03 mg Zn/kg ww (M. gigas). The one-way ANOVA analysis also indicated that crustaceans significantly (pP. monodon), and 11.71 mg/kg ww (S. paramamosain), respectively. The differences in metal accumulation among marine species could be related to each species’ unique physiology and ecological niches [
39].The rank order of the average heavy metal accumulation in the edible tissues of all collected seafood species from Pattani Bay was shown in
Table 2. The top-ranking essential metal in most species was either Fe or Zn. Iron and Zn are essential trace elements for biota. Molluscs have a high content of Fe as it is a constituent of goethite (α-FeOOH) for the proper functioning of radula [
40]. Whereas, Zn is of major importance in metabolic processes: it is a constituent of haemocyanin, hence the level of this element will be higher [
40]. Cadmium and Co are toxic elements commonly found at the lowest concentrations. Their levels in seafood species in this study correspond to a previous study and are relevant to the levels found in the environment [
6]. Hence the lowest concentrations were observed in animal tissues. Average concentrations of nine heavy metals decreased in the sequence of molluscs > crustaceans > fish. A similar order of heavy metal accumulation was also observed in organisms from other regions, such as Laizhou Bay, China [
16,
41], and Saint Martin Island, Bangladesh [
12]. Marine organisms can directly accumulate heavy metals from water and sediment. There is a strong correlation between heavy metal accumulation in marine species and their habitats, especially if they are in close contact with sediments [
42,
43,
44]. The blood cockle (T. granosa), Asiatic hard clam (M. meretrix), Asian green mussel (P. viridis), common geloina (P. erosa), Pacific oyster (M. gigas), and giant tiger prawn (P. monodon) are species that usually feed on sediment. Their feeding method can contribute to a more significant accumulation of heavy metals than other marine species. Molluscs, especially the filter-feeding animal bivalves, are well-known for their active ingestion of heavy metal-bound organic and inorganic matter. These bivalves can also highly expose to heavy metals during feeding and accumulate a wide range of metals from sediments [
45,
46]. Moreover, marine organisms can readily assimilate and accumulate the freely dissolved and transported heavy metals in seawater [
47]. Among the four studied fish species, M. cephalus and S. argus are herbivores whereas N. thalassina and P. lineatus are limnivores or mud-eating. From one-way ANOVA analysis, S. argus significantly (p
12,
16,
48,
49]. Exposure of various marine species to heavy metals, mainly Cd, Cu, and Zn is associated with the induction of metallothionein. Metallothionein (MT) is a cysteine-rich, low-molecular weight protein that plays a special part in regulating the intracellular homeostasis of essential and non-essential metals, and their detoxification [
50,
51,
52]. Thus, the excess heavy metals will be detoxified by metallothionein and stored in tissues including the liver, kidneys, and muscle. Heavy metal accumulations were observed in the edible tissues of fish (muscle), molluscs (body tissues containing visceral elements), and crustaceans (body and claw tissues) in this study. However, heavy metal concentrations observed in molluscs and crustaceans were higher than in fish. The biomagnification process through the food chain resulted in high levels of heavy metals in higher trophic organisms [
53,
54,
55,
56,
57,
58]. Our findings provide the association between heavy metal accumulation in seafood tissues and their feeding patterns. To avoid health risk effects, consumers should select fish as food instead of molluscs or crustaceans which are more likely to be exposed to heavy metals.Both national and international permissible limits of heavy metals have been established to ensure food safety and security for human consumption, except Cd, Fe, and Mn [
29,
59,
60]. The concentrations of investigated heavy metals in selected seafood species varied among species (
Figure 2). The FAO recommends limits of Cr and Ni for seafood of 12 mg/kg ww and 70 mg/kg ww whereas USFDA set the permissible levels at 13 mg/kg ww and 80 mg/kg ww, respectively [
28,
30]. Accumulations of Cr and Ni in all seafood species were below both the FAO and USFDA permissible limits [
28,
30]. The maximum Cd limit in Thailand is 1 mg/kg ww for fish, whereas the limit of CODEX is 2.00 mg/kg ww for bivalve molluscs [
25,
29]. Cadmium concentrations found in all fish, molluscs, and crustaceans in this study were below both Thailand and CODEX permissible levels. Copper concentrations detected in crustaceans except F. merguiensis exceeded the EU limit of 5 mg/kg ww [
27]. In contrast, its levels in fish were well below the FAO permissible levels of 30 mg/kg [
28]. Copper, an essential element, is easily absorbed by aquatic organisms. This is relevant to the relatively high content in these seafood species [
61]. The above limit Cu was also observed in oysters (42.89 mg/kg) [
62] and shrimps (5.67 mg/kg) [
61]. Copper plays significant roles in the immune, hematopoietic, and cardiovascular systems, and in oxidative stress control [
63]. However, excessive Cu can cause gastrointestinal distress and harm the the liver, immune, neurological, and reproductive systems [
63]. Iron (Fe) was the most abundant trace element found in all tissue samples ranging from 2.44–227.72 mg/kg ww. Its high concentration in samples indicates that the environment was stressful [
64]. Manganese is also an essential element, and its deficiency could lead to severe skeletal and reproductive abnormalities in mammals [
65]. Molluscs, in this study, accumulated the highest concentration of Mn (7.04 mg/kg ww; P. erosa). Lead, a non-essential element, is well-known for its adverse health effects [
60]. Its concentrations in this study ranged from 1.68 to 11.71 mg/kg ww, which were more significant than the maximum EU, FAO, and WHO permitted levels of 1.44, 2.4, and 9.6 mg/kg ww, respectively [
26,
28,
31]. In addition, high concentrations of Pb were recorded from the topsoil of the Pattani River mouth (557.15 mg/kg), resulting in high Pb contamination in Pattani Bay (6.43–69.49 mg/kg). This can increase the risk to aquatic animals and local human health [
6]. Present findings showed that Pb concentrations in detected seafood species were relatively high for human consumption. Acute exposure to high Pb levels can cause gastrointestinal, renal, and brain damage along with other toxic effects [
66]. Zinc, an element essential for metabolic processes, was also found in all samples. Most Zn concentrations in all species were below the permissible of 100 and 1000 mg/kg ww set by WHO, for fish and crustaceans, respectively [
67,
68], except for M. gigas (198 mg/kg ww).Average heavy metal accumulation in fish, molluscs, and crustaceans is shown in
Figure 3. The paired sample t-test indicated that seasonal and collecting location variations affected heavy metal concentrations in seafood tissues. Seasonal variations affected heavy metal accumulation for most studied heavy metals except Mn. Fish showed significantly higher concentrations (ppp
60].Seasonal fluctuations of heavy metals can result from several factors, such as growth, organismal reproductive cycles, and water temperature changes. These factors could contribute additional factors that affect metal bioavailability in marine organismal tissues [
69,
70,
71]. Studies linked to the reproductive cycle can explain the essential seasonal variations of heavy metal bioaccumulation in mollusc tissues [
70,
71]. Marine animal gonads are increased enormously during gametogenesis and could constitute an effective trap for incorporating metals into living organisms. This is related to cellular energy mainly used in gamete production [
59]. Our results showed high Cu, Pb, and Zn concentrations in molluscs during the dry season. This coincided with gametogenesis processes taking place during such a period. The present study also found a higher concentration of Ni and Pb in fish tissues and Cd, Co, Cu, Fe, Ni, and Pb in crustacean tissues during the dry season, similar to other studies [
72,
73,
74]. Fish and shrimps increase their physiological motion in the dry season which could produce a higher accumulation of heavy metals [
75]. The growth rate of fish is higher in summer, and can thus result in greater heavy metal accumulation [
76]. The gradual accumulation of nutrients during the pre-spawning season in dry season could introduce significant variations of metal concentrations and metallothionein content in the digestive gland due to the “biological dilution” effect [
77]. Therefore, these can also increase heavy metal accumulation in tissues during the dry season. Our findings provide evidence that most heavy metals accumulated in seafood tissues during the dry season were higher than in the wet season. This finding would suggest that seafood consumption during the wet season would cause lower health risk effects than in the dry season. The monitoring of heavy metals contaminated seafood should periodically be performed to prevent health risks of consumers, especially those in the surrounding areas.
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