Concentrations of Heavy Metals in Muscle with Relationto the Growth of Two Marine Fish Species

Le Quang Dung, Nguyen Viet Linh, Nguyen Xuan Thanh, Nguyen Duc Cu, Vu Van Tu3, Takaomi Arai

1. Institute of Marine Environment and Resources, Vietnam Academic of Science and Technology, Haiphong, Vietnam 2. Institute of Oceanography and Environment, Universiti Malaysia Terengganu, Kuala Terengganu, Malaysia 3. Institute of Environmental Technology, Vietnam Academic of Science and Technology, Hanoi, Vietnam



Concentrations of Heavy Metals in Muscle with Relationto the Growth of Two Marine Fish Species

Le Quang Dung1,2,*, Nguyen Viet Linh1, Nguyen Xuan Thanh1, Nguyen Duc Cu1, Vu Van Tu3, Takaomi Arai2

1. Institute of Marine Environment and Resources, Vietnam Academic of Science and Technology, Haiphong, Vietnam 2. Institute of Oceanography and Environment, Universiti Malaysia Terengganu, Kuala Terengganu, Malaysia 3. Institute of Environmental Technology, Vietnam Academic of Science and Technology, Hanoi, Vietnam

Received 29 September 2013 accepted 4 November 2014

Heavy metal concentrations in muscle and their relation to thegrowth of two marine fish species, including tonguefish (Cynoglossusarel) and mullet (Mugilcephalus), were studied. The samples were collected in Bach Dang estuary andconcentrations of heavy metals (As, Cd, Co, Mn, Cu, Zn, Pb, and V) in muscle of the fisheswere determined. The result showed that the accumulated trend of heavy metal is different between fish species. The concentration of As, Zn, Mn, V, Cu, Pb, Co and Cd in tonguefish were 73.7±30.6, 22.82±4.87, 3.44±2.13, 1.61±0.15, 0.71±0.13, 0.45±0.24, 0.03±0.02 and 0.02±0.02 mg·g-1, respectively. Meanwhile the concentration of Zn, As, V, Mn, Cu, Pb, Co and Cd in mullet were 83.41±19.68, 9.78±1.92, 1.36±0.54, 1.29±0.51, 0.65±0.12, 0.42±0.20, 0.06±0.03 and 0.03±0.01mg·g-1, respectively.Comparison of metal levels among thesespecies indicated that the concentrations of As and Mn in tonguefish were significantly higher than those in mullet, whereas Zn levels in mullet were found to be higher than that in tonguefish. There is no significant differences of Cd, Co, Cu, Pb and V levels in muscle between two species.Significant inversed relationshipsbetween concentration levels of metals and lengths of tonguefish were found for Mn, Cu and Zn, butnot for As, Cd, Pb, and V. There were no significant relationships between the heavy metal concentrations and the length of mullet. In general, decreasesof the heavy metal concentrations corresponded to the increases of fish body lengths, particularly for As, Co, Cu, Mn and V and the exception for Cd.Terefore reduced risks were associated with consuming biggermullet fish, and increased risks of As and Cd were associated with consuming bigger tonguefish in Bach Dang river mouth.

heavy metals; concentration levels; marine fish; health risk; Vietnam

Bach Dang is one of the biggest river mouths belong to Red River Delta system in Vietnam, which contains diverse of habitats that support an abundance of marine life and their spawning grounds and nurseries. However, with the increased urbanization and industrialization, there has been a rapid increase in the municipal waste water (sewage water and industrial effluents) which has potentially caused the environmental pollution along the coast in recent[1]. Among pollutants, heavy metals are great concern because of their toxicity, persistence and prevalence. Though some metals, such as Cu, Zn and Co, are known to be essential elements and play important roles in biological metabolism at very low concentrations, they become poisonous when their concentrations exceed the metabolic requirements. Others are known to be toxic even at low concentrations, including As, Cd, Hg, Pb etc. Heavy metals can enter aquatic organisms through the food web and they can magnify in animals via food chain such as mercury, cadmium[2]. Therefore, fish, the top predators in marine ecosystem, often has been concerned of metal bioaccumulation in a number of studies for years, because fishes provide important proteins and omega-3 sources for human and metal contaminations in fish can threaten human health for consumption and other fish consumers. Studies on fish showed that accumulation of heavy metals in tissues is not only mainly dependent upon metal concentrations in water or exposure period, but other environmental factors, salinity, pH, hardness and temperature, also influence in metal accumulation[3]. Furthermore, physiological conditions of fish, such as sex, size, age and growth stages, were found to affect the metal accumulation in its tissues[4-5].

The sizes of fish were shown to play an important role in metal contents of tissues. There was evidence that the concentration of certain metals sometimes either increases or decreases significantly with body size, however this was not always the case[6-7]. The cadmium concentration in the muscle tissue increased with increasing body weight ofIctaluruspunctatus, it decreased inMinytremamelanops, whereas copper levels in muscle of fish showed no correlation with body size from the Savannah River[7]. The concentration of nine different heavy metals in muscle tissue either declined or remained relatively constant with increasing body weight of five fish species from the Swan-Avon river system[8].

A number of studies on heavy metals in Vietnam waters have been reported[1-9]. However, studies on heavy metal accumulation in marine fish are still limited and no recentdata published on the relationship between level of heavy metals in fish tissues and body sizes fromVietnam coastal waters. The previous studies mainly investigated concentrations of heavy metal in water or sediments[1,9-10]. Several studies examined the content of heavy metals in the clam, mussel, shrimp[11].

Therefore, the aim of this study was to determine the residues of heavy metals in edible muscle tissue, and to explore the relationship between metal accumulation and body size of two marine fish species,MugilcephalusandCynoglossusarel. These two species are widely distributed in Vietnam coastal waters and they are also common commercial value as seafood for local people.

1 Materials and Methods

1.1 Sampling

Tonguefish (Cynoglossusarel) and mullet (Mugilcephalus) were caught by trawling netin March 2012 from Bach Dang river mouth (Figure 1).M.cephalusis pelagic, whereasC.arelis benthic fish.Twenty fishes of each species were collected with different body size to exam the relationship between metal levels in muscle and total length. During sampling, fish samples was transported by icebox. Total length (mm) and body weight (g) were measured for each fish. Muscle tissues were dissected out, weighed, put in clean polyethylene bags and stored at -20℃ in freezer before chemical analysis.

1.2 Chemical analyses

Fish tissues were dried to constant weight before grinding into powder. The dried tissue samples were digested in a Teflon bomb by a microwave oven as described in a previous study by Le et al[12]. The digested solutions were diluted with 30 mLMilli-Q water (Milli-Pore Company) into polyethylene and stored at 4℃ until metal measurement.

Fig. 1 Fish sampling in Bach Dang estuary: (●) where M. cephaluswas collected; (■) where C. arel was collected

Before measuring eight elements of heavy metals (As, Cd, Co, Mn, Cu, Zn, Pb, and V) in fish samples by inductively coupled plasma mass spectrometer (ICP-MS) (ELAN 9000 Perkin Elmer, USA), internal standard solution including Scandium (Sc), Indium (In), and Bismuth (Bi) was added to each sample to correct the matrix effects and instrumental drift in ICP-MS during measurement. The accuracy of the method was assessed with standard reference materials, DORM 3 (National Research Council, Ottawa, Canada). Recoveries of As, Cd, Cu, Pb and Zn were 86.5%, 89.5%, 100.4%, 86.4% and 91.4%, respectively.

Detection limits of As, Cd, Co, Mn, Cu, Zn, Pb, and V were estimated to be 0.001, 0.0001, 0.0001, 0.001, 0.001, 0.01, 0.0001, 0.0001mgg-1, respectively.

1.3 Statistical analysis

The results were calculated by Microsoft excel and expressed as meanSD. Significant relationship was estimated between the metal concentrations and total length of fish by Pearson correlation coefficient. The statistical relationships were performed using SPSS ver. 20.

2 Results

2.1 Biological information

The total length and weight (mean±SD) of two fish species are given in Table 1.The body size of tonguefish is ranged from 12.1～21.5 cm length and 7.5～39.2 g weight, while mulletis from 13.5～19.3 cmlengthand 20.8～79.7 g weight.

Table 1 Biological information of 2 fish species

2.2 Metal levels in fish species

The mean concentrations (mg·g-1) of the nine heavy metals in the fish muscle are shown in Table 2. The accumulated trend of heavy metal is different between fish species. Arsenic content (73.7±30.6 mg·g-1) was highest in tonguefish, followed by Zn (22.82±4.87 mg·g-1), Mn (3.44±2.13 mg·g-1), V (1.61±0.15 mg·g-1), Cu (0.71±0.13 mg·g-1), Pb (0.45±0.24 mg·g-1), Co (0.03 ± 0.02 mg·g-1) and Cd (0.02±0.02 mg·g-1). Meanwhile Zn (83.41±19.68 mg·g-1) was found to be the highest level in mullet, followed by As (9.78±1.92 mg·g-1), V (1.36 ± 0.54 mg·g-1), Mn (1.29±0.51 mg·g-1), Cu (0.65 ± 0.12 mg·g-1), Pb (0.42±0.20 mg·g-1), Co (0.06±0.03 mg·g-1) and Cd (0.03±0.01mg·g-1).

Table 2 Biological information of 2 fish species

Comparison metal accumulations between two species showed that the levels of As and Mn in muscle of tonguefish were significantly higher than those in mullet (Tukey HSD test for equal N, P0.05). Whereas Zn levels in mullet were found to be higher than that in tonguefish(Tukey HSD test for equal N, P0.05). There is no significant difference of Cd, Co, Cu, Pb and V levels in muscle between two species.

2.3 Relationship between metal levels and body size

Correlation between trace metal levels and total length of fish species are presented in Table 3. For tonguefish C. arel, inversely significant correlations are found between Mn, Cu and Cr levels with total length, the coefficients are R=-0.88, -0.94 and -0.98, respectively. Although no significant correlation is found between the levels ofAs, Cd, Pb and V with total length (P>0.05), the trends of the heavy metal accumulation are different. While As and Cd tended to increase with increasing body size, V and Pbshow the decreased trend. Cobalt does not expose any trend with total length of the fish.

Table 3 Relationship coefficience between metal

For M. cephalus, significant correlation is found between Co and V in mucle and total length, the coefficients are -0.63 and -0.68, repectively. There is no correlation between the remained heavy metal levels with total length, however, the concentrations of As and Zn tend to decrease with increasing body size, and Mn, Co and Cd show opposite trend.

3 Discussion

A number of studies resulted that different fish species contained strikingly different metal levels in their tissues[13-14]. However, in present study, similar levels of Cd, Cu, Pb and V levels in muscle were found between species. This might reflect the exposure of the same metal levels in the sampling site and similar metabolism of these metals in the fishes. The difference of metal level between species found were As, Co, Zn and Mn. Among them, Co, Mn and Zn were known as essential metals for living organisms, the difference of these metal levels between species might relate to requirement of metal intake during metabolic processes. Whereas the different levels of As, known as non-essential metals for fish, mightresult from the different exposurefrom foraging habits of the two species. M. cephalus are pelagic, they feed on detritus, diatoms, algae and microscopic invertebrates which they filter from surface sediment through their mouth and gills[15].C. arelare benthic fish, they are purely carnivorous, their food items mainly polychaeta, creatacean and molluscs[16].Total arsenic levels increased with higher trophic level in marine ecosystem[17]. Additionally, Goessler et al[18]suggested that arsenic could be biomagnificated through food chain, the concentrations of As increased from algae, to zooplankton, to forage fish, to predator fish. Although As was known as poinson in inorganic form, As existed in marine fish or seafood were mainly in organic forms, such as arsenobetaine, arsenoribosides, and arsenocholine, they are effectively non-toxic[19]. Pershut et al[19]stated that inorganic arsenic in fish muscle tissue was very low, ranged from below detected limition to lower than 3% of total arsenic. Additionally, the study also indicated that benthic feeding regime was more important than a pelagic one for arsenic ingestion.

For relationships between heavy metal concentrations in fish with fish size, due to As accumulated in organic form presented less health hazard as compared to inorganic As in marine organisms, they could rapidly excrete organic form of arsenic[20-21]. Furthermore, difference of food items between species as discussed above plus metabolic rate of the fish. These could partly explain the different trends of As accumulated levels in the 2 fish species with the total length.

For other heavy metals, non or negative correlations found between metal levels in muscle and body sizes of fishes were generally supported byprevious studies[7-8-22-23]. Nussey et al[22]showed that accumulation of metals (Cr, Mn, Ni, and Pb) decreased with the increasing length of fish Labeoumbratus. Widianarko et al[23]also found that there was a significant decline in Pb concentrations with the increase in size of fish (Poeciliareticulata), whereas concentrations of copper and zinc did not depend on body weight. They indicated that body concentrations of copper and zinc are regulated and maintained at a certain concentration. In the present study, the decreasing trend of the essential metal levels, Co, Mn, Cu and Zn, in the larger size of fish might relate to the metabolic ratesor influence body burdens of metal due to a growth dilution effect. Because the concentrations of these metals in the fishes werewithin the normal physiological range when they were comparable with results of Fezal et al[14]for C. arel andCanli and Atli[6]for M. cephalusin less polution areas.

Levels of nonessential metals, Cd, Pb, and V, were showed no correlation with total length, except V was inversely correlated with body size of tonguefish C. arel, however these all metals resulted similar trends of accumulation betweenthe species. V and Pbshowedthe decreasing concentrations with increasing body size, whereas Cd tended to slightly increase concentraitonin the larger fish. The difference of accumulated trendsbetween the heavy metals couldnot only relate to the elimination rate of pollutants from fish, but also depended on the metal-specific chemistry[24]. In marine fish, Fundulusheteroclitus, cadmium slowly excreted through kidneyand 90% of the Cdlost during a 6-month posttreatment observation period[25]. Furthermore, Hervé-Fernández et al[26]conducted a experiment to exam the depuration rate for accumulated Cd in blue mussels (Mytiluschilensis). He found that only 21% of the total accumulated in the whole mussel being eliminated after 52 days.Meanwhile, biological half-life of Pb was about 25 days in blood and it had a longer half-life of about 40 days in the muscle[27]. Canli and Atli[6]also found that no correlation between Pb levels in muscle of M. cephalus with weight, however declined trend of Pb levels in muscle with increasing weight was reported. In case of vanadium, although V was the one of few heavy metals known to be enriched in marine waters through anthropogenic input[28], few studies have examed the bioaccumulation of V in marine teleost fish. Little information on relationship between V levels in mucle and body size of fish in wild was available to compare with this study. Miramand and Fowler[29]stated that marine organisms generally did not highly accumulate vanadium from environmental media, and there was no indication of biomagnification in food chains. He added that V was rapidly lost after accumulating in tissues of marine organisms[30-31]. Some experimental studies indicated that bioliogical half-life of V in benthic fish (Gobius minutus) was within 3 days[31], and in a bivalve feeding on suspended matter (Mytilus galloprovincialis) was 7 days[30]. These might partly explain the the declined trend of V in mucles of the marine fishes with increasing body size.

Overall, this study concludes that metal levels varied significantly among species might relate to fish’ food items and metabolic processes, the negative relationships between metal contaminant load and body sizes would indicate that risk could be reduced by consuming larger mullet fish, whereas trends of As and Cd levels with increasing body size of tonguefish should be concerned for consumers from Bach Dang river mouth.

ACKNOWLEDGMENT:The authors would like to thank colleagues for kind help during sampling in field and laboratory work.

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1673-5897(2015)3-304-07

X171.5

A

10.7524/AJE.1673-5897-20130909001

The study was supported by Vietnam Academic of Science and Technology, No. VAST.DT. 06/12-13, and by the Asian CORE Program of JSPS. Bibliology： Le Quang Dung, PhD. Researcher in Institute of Marine Environment and Resources and Lecturer in University Malaysia Terengganu Email:lqdungimer@gmail.com

Le Q D, Nguyen V L, Nguyen X T, et al. Concentrations of heavy metals in muscle with relation to the growth of two marine fish species [J]. Asian Journal of Ecotoxicology, 2015, 10(3): 304-310 (in Chinese)