An Assessment of Heavy Metal Bioaccumulation in Asian Swamp ...

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Abstract Livers and muscles of swamp eels (Monopterus albus) were analyzed for bioaccumulation of heavy metals during the plowing stage of a paddy cycle.

Bull Environ Contam Toxicol DOI 10.1007/s00128-013-1009-4

An Assessment of Heavy Metal Bioaccumulation in Asian Swamp Eel, Monopterus albus, During Plowing Stages of a Paddy Cycle Ai Yin Sow • Ahmad Ismail • Syaizwan Zahmir Zulkifli

Received: 6 March 2012 / Accepted: 26 April 2013 Ó Springer Science+Business Media New York 2013

Abstract Livers and muscles of swamp eels (Monopterus albus) were analyzed for bioaccumulation of heavy metals during the plowing stage of a paddy cycle. Results showed heavy metals were bioaccumulated more highly in liver than muscle. Zinc (Zn) was the highest bioaccumulated metal in liver (98.5 ± 8.95 lg/g) and in muscle (48.8 ± 7.17 lg/g). The lowest bioaccumulated metals were cadmium (Cd) in liver (3.44 ± 2.42 lg/g) and copper (Cu) in muscle (0.65 ± 0.20 lg/g). In sediments, Zn was present at the highest mean concentration (52.7 ± 2.85 lg/g), while Cd had the lowest mean concentration (1.04 ± 0.24 lg/g). The biota-sediment accumulation factor (BSAF) for Cu, Zn, Cd and nickel (Ni) in liver tissue was greater than the corresponding BSAF for muscle tissue. For the three plowing stages, metal concentrations were significantly correlated between liver and muscle tissues in all cases, and between sediment and either liver or muscle in most cases. Mean measured metal concentrations in muscle tissue were below the maximum permissible limits established by Malaysian and U.S. governmental agencies, and were therefore regarded as safe for human consumption. Keywords Heavy metals  Bioaccumulation  Plowing stages  Swamp eel

The presence of heavy metals in the environment and foods is a major concern of the community. One of the efforts to monitor pollutant levels in the environment is by using bioindicators. This approach has been widely used to A. Y. Sow  A. Ismail (&)  S. Z. Zulkifli Department of Biology, Faculty of Science, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia e-mail: [email protected]

monitor the levels of pollutants in specific areas. In Malaysia, several organisms have been proposed as bioindicators, such as Perna viridis (Ismail 1990), Oryzias javanicus (Khodadoust et al. 2013), Telescopium telescopium (Ismail and Safahieh 2005), Nerita lineata (Ismail and Ramli 1997), Uca annulipes (Ismail et al. 1991), Dotilla myctiroides (Zulkifli et al. 2012a), Thais spp. (MohamatYusuff et al. 2010, 2011), Anguilla bicolor bicolor (Arai et al. 2012) and Periophthalmodon schlosseri (Ikram et al. 2010; Zulkifli et al. 2012b). These bioindicators are reported in the form of their changes (biochemical, physiological or behavioral) due to exposure and the bioavailability of pollutants that exist in the surrounding environment. Paddy fields are important agricultural lands that supply rice for human consumption, particularly in Asia. In order to optimize the growth and production of rice, agrochemical pesticides and fertilizers are applied into paddy fields. Excessive application of these chemical compounds may introduce significant amounts of pollutants, including heavy metals into the paddy field areas. This may affect non-target organisms. The Asian swamp eel (Monopterus albus) is one of the common and important fish species that exists in paddy field areas. Spawning of this species can occur throughout the year. Eggs are laid in free-floating bubble nests amongst the submerged vegetation near the male’s burrow (Sadovy and Shapiro 1987). Females produce up to 1,000 eggs per spawning event (Chivers 1999). This fish is believed to migrate to other areas whenever excessive pesticides are being applied by farmers. They may return to the paddy field area during the flooding stage (initial process of a paddy cycle). Plowing, which is the second process of the cycle can be divided into three stages (I, II, and III). On average, each stage takes about 1 month to be completed. This process is important to break and turn over the soil. Standing water during the flooding stage flattens

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the soil and reduces soil permeability. As a result, the plowing process could potentially resuspend pollutants that exist from previous paddy cycles in the deep soil layers. In turn, the resuspended pollutants may be bioaccumulated into existing living organisms (Zulkifli et al. 2010a). Sediments are depositional areas for physical and biological debris, and sinks for a wide variety of chemicals (Zoumis et al. 2001). In the paddy field system, anthropogenic sources of metals have been identified as the major pathway for their introduction into the ecosystem (Wang et al. 2003). It has also found that some metals may be transformed into other species once they have entered the environment (Lu et al. 2005). Lu et al. (2005) also explained the transformation usually from the loosely bound fraction (such as exchangeable fraction) to strongly bound fractions (such as Fe–Mn oxide and organic matter bound fractions). In this study, repetitive application of agrochemical pesticides and fertilizers, atmospheric deposition and naturally available metals from soils, may contribute to the levels of heavy metals in paddy soils. Since most heavy metals are persistent and toxic materials, they may exert harmful effects if present above specific thresholds of tolerance (Sow et al. 2012a). When they are introduced into the aquatic environment, they can either be adsorbed onto sediment particles or bioaccumulated in aquatic organisms (Mohamed Fatma 2008). Swamp eels are among the commonly found in paddy fields, and are consumed by local residents. Since they are closely associated with the sediment, the potential is high for them to accumulate pollutants, especially if the pollutants are resuspended during the plowing and cultivating stages. The biota-sediment accumulation factor (BSAF) is a useful measure for evaluating the uptake and incorporation of pollutants into their tissues. The BSAF for metals is defined as the ratio of metal concentration in the organism to the concentration in sediment (Lau et al. 1998; Szefer et al. 1999). It is calculated as BSAF ¼ MðtissueÞ =MðsedimentÞ where tissue and sediment both are expressed on a dry weight basis. This study was conducted to determine the bioaccumulation of selected heavy metals in the swamp eel during the three plowing stages of a paddy cycle. Metal concentrations in the eel tissues were evaluated relative to permissible limits established by governmental agencies.

Materials and Methods Samplings were conducted in a paddy field area in Tumpat district (located in the northeast of Peninsular Malaysia: N 06°08.4540 E 102°08.4300 ) as illustrated in Fig. 1.

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Sampling activities were conducted monthly (March–May 2011) during the plowing stage of a paddy cycle. A total of 38 individuals of M. albus and 27 replicates of paddy field soils were collected. Due to their sequential hermaphrodite status (Shafland et al. 2010), sexual classification was not conducted. A trap was placed in the paddy field for a day with a small amount of artificial bait (cooked fish) placed inside. The trap was checked on the following day for the presence of M. albus. The collected eels were placed into polyethylene plastic bags. Surface sediments in the vicinity of the traps were collected and stored in polyethylene plastic bags. All samples were transported back to the laboratory and stored in a freezer at -20°C until further analysis. Prior to dissection, each eel was weighed and measured for standard body length. The average body weight and standard body length were 104.3 g and 46.6 cm. Each eel sample was dissected to obtain the liver and muscle tissues. All samples were dried in an air-circulating oven at 60°C for 72 h until a constant dry weight (dw) was obtained. Dried sediments were sieved through a 63 lm mesh stainless steel sieve to produce homogeneity. Sample digestion was conducted based on the method described by Ismail (1993) and Ismail and Ramli (1997). For liver and muscle samples, about 1 g of sample was digested with 10 mL concentrated HNO3 (AnalaR grade, BDH 69 %). Digestion was accelerated by heating on a hot block digestor at 40°C for 1 h, followed by heating at 140°C for 3 h. Sediment samples (*1 g) were digested with a mixture (4:1, v/v) of HNO3 (AnalaR grade, BDH 69 %) and HClO4 (AnalaR grade, BDH 60 %) as described by Ismail (1993). Digestion with heating was performed as described above. Once the digestion was completed, samples were left to cool to room temperature. Ultrapure water was added into the sample to a fixed volume. Each sample was then filtered through Whatman No. 1 filter paper. All samples were analyzed by using an air-acetylene flame atomic absorption spectrophotometer (Perkin-Elmer Model AAnalyst 800, Shelton, CT, USA) for Zn, Ni, Cu and Cd concentrations. Multiple-level calibration standard solutions were analysed to generate calibration curves. For quality measures, all glassware and equipments were acidwashed prior to use. For the accuracy of analytical procedures, certified reference material (CRM) for soil (PACS2) and fish (DORM-3) (NRCCNRC, Canada) were analyzed along with the samples. The recoveries were 75.4 %–114 % for PACS-2 and 78.1 %–103 % for DORM-3, as shown in Table 1. The data obtained from analyzing were converted and expressed as lg/g dry weight basis. Statistical analysis of data was carried out by using IBM SPSS statistical package version 19 (Armonk, New York, USA). One-way ANOVA and Tukey’s post hoc test were applied to compare the mean of metals concentrations by different plowing stages.

Bull Environ Contam Toxicol Fig. 1 Sampling locations of M. albus in paddy fields around Tumpat, Kelantan (Malaysia)

Table 1 Certified and measured concentrations of metals (lg/g dry weight) in fish tissue and sediment Metal

Certified value (lg/g)

Measured value (lg/g)

Percentage of recovery (%)

DORM-3 Cu

15.5 ± 0.63

16.0

Zn

51.3 ± 3.10

47.9

103

Cd

0.29 ± 0.02

0.30

Ni PACS-2

1.28 ± 0.24

1.00

78.1

Cu

310 ± 12.0

262 ± 4.55

84.5

Zn

364 ± 23.0

274 ± 4.74

Cd

2.11 ± 0.15

2.40 ± 0.12

Ni

39.5 ± 2.30

37.5 ± 0.94

93.4 103

75.4 114 95.0

Pearson’s correlation test was applied to determine the extent to which metal concentrations in sediment, liver and muscle were correlated with one another. This test was applied to different plowing stages, namely March (I), April (II), and May (III).

Results and Discussion The ranges for mean concentrations of Cu, Zn, Ni and Cd in sediment were 27.0–31.6, 42.5–64.0, 10.3–20.5 and 0.73–1.61 lg/g (dry wt) respectively (Table 2). Concentrations of these metals during stage 1 plowing were found to be at the highest concentration, as compared to other

stages. However, only concentrations of Zn and Ni were significantly different amongst the three plowing stages (p \ 0.05). In the present study, Zn had the highest concentration in the sediment and Cd the lowest. Similarly, Zn was found to have the highest concentration based on the report by Zulkifli et al. (2010b) in a nearby area. High Zn levels in paddy soil could be due to the clayey nature of the paddy soil. Mancheau et al. (2005) reported that Zn in acidic to near-neutral aluminium-rich paddy soils in Vietnam with high clay content was predominantly bound to the hydroxyl-Al interlayers in the fine soil matrix, which provided a good binder for Zn accumulation. The low concentration of Cd in Tumpat paddy soil may indicate fundamentally low concentrations in the soil materials of this region. This could be due to Cd removal from the soil by leaching and crop uptake (Mattson et al. 2000). Some Cd may be added from the occasional use of rock phosphate fertilizers by farmers during the plowing season, as these are known to be a source of Cd (Sabiha-Javied et al. 2009). A similar pattern of low Cd concentrations in paddy soil was observed by Khairiah et al. (2009) from the states of Kedah and Perlis, Malaysia. If all concentrations of the selected metals are compared with the sediment quality guidelines proposed by Long et al. (1995), current levels in the paddy soil should not pose a threat to existing organisms. Table 2 shows that mean concentration of Cu, Zn and Ni are below the effect range low (ERL), thus indicating that effects on aquatic life of present concentrations for these metals in sediment are not likely to occur. The concentrations of Cd in the sediment exceeded the ERL value, but were well below the

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Bull Environ Contam Toxicol Table 2 Mean concentrations of metals (lg/g dry weight) in liver and muscle samples of M. albus and surface sediments from a paddy field in Tumpat, Malaysia during three plowing stages Sample

Plowing stage

Cu

Liver

1

7.13 ± 2.00ab

2 3 Muscle

Sediment

9.23 ± 2.78

a

6.68 ± 2.47

b

Cd

94.9 ± 14.0a a

108 ± 25.5

92.4 ± 7.87

a

Ni

1.78 ± 1.23b

23.1 ± 19.5a

a

4.64 ± 2.71b

b

2.16 ± 0.95

0.16 ± 0.08b

6.37 ± 5.28

Mean

7.68 ± 0.39

98.5 ± 8.95

3.44 ± 2.42

9.28 ± 10.5

1

0.84 ± 0.56a

59.3 ± 10.9a

1.61 ± 1.12a

19.7 ± 15.1a

2

0.95 ± 0.27

a

a

a

1.55 ± 0.43

1.43 ± 0.38b

3 Mean

0.15 ± 0.17b 0.65 ± 0.20

27.7 ± 21.0b 48. 8 ± 7.17

0.38 ± 0.19b 1.18 ± 0.48

0.04 ± 0.00b 7.06 ± 8.59

1

31.6 ± 4.33a

64.0 ± 7.61a

1.61 ± 0.51a

20.5 ± 2.46a

2

27.0 ± 2.69

b

51.6 ± 3.07

b

b

10.3 ± 1.47c

30.0 ± 1.27

a

42.5 ± 2.36

c

b

0.77 ± 0.08

13.9 ± 0.80b 14.9 ± 0.84

3 Sediment quality guideline (Long et al. 1995)

Zn

59.4 ± 7.12

0.73 ± 0.10

Mean

29.6 ± 1.53

52.7 ± 2.85

1.04 ± 0.24

Effect range low (ERL)

34

150

1.2

20.9

Effect range median (ERM)

270

410

9.6

51.6

Post-hoc: Mean metal concentrations of sediment, liver and muscle sharing a common letter for a particular metal are not significantly different, p [ 0.05

effect range median (ERM), indicating that concentrations of this metal in the sediment may occasionally result in adverse effects on aquatic life. However, more data are needed to support these findings. The mean concentrations of selected heavy metals in liver and muscle of M. albus are listed in Table 2. In general, bioaccumulation of Cu, Zn, Cd and Zn was found to be higher in liver than that in muscle of M. albus. Bioaccumulation of these metals in liver was significantly different than in muscle (p \ 0.05). The highest bioaccumulated metal in liver was Zn (98.5 ± 8.95 lg/g), while Cd (3.44 ± 2.42 lg/g) was the lowest bioaccumulated metal. As for muscle, Zn (48.8 ± 7.17 lg/g) was the highest bioaccumulated metal, while Cu (0.65 ± 0.20 lg/g) was the lowest bioaccumulated metal. Zn is required to support important biological functions and a relatively high level is necessary to maintain these vital functions (Ahdy Hoda et al. 2007). According to Oehlenschlager (1997), Zn is a constituent of all cells and of many enzymes. A similar pattern was reported by Kargin (1996). The source of Zn for uptake by the eels may be from the partitioning of Zn from the sediment or water, as well as uptake from food. For decades, the liver has been assumed to be a major target organ for metal bioaccumulation because it is a metabolically active tissue which has been found to accumulate metals to high levels in both experimental (Allen 1994; Kalay and Erdem 1995) and field studies (Karadede ¨ nlu¨ 2000). Our study was in agreement with these and U findings. Table 2 also showed Cu and Cd were less highly bioaccumulated than Zn and Ni. A study by Mokhtar et al. (2009) on Oreochromis spp. reported the mean

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concentration of bioaccumulated Cu in this fish was 0.31 ± 0.04 and 0.32 ± 0.02 lg/g, respectively in liver and muscle. As for Cd, the bioaccumulated concentrations were 0.02 and 0.01 lg/g in liver and muscle respectively. By comparing results from the present study with that of Mokhtar et al. (2009), concentrations of Cu and Cd in muscle and liver tissues during the plowing season of our study were higher in most cases. The chemical fertilizers, which contain significant amounts of Zn and Cu forms may have contributed to higher concentrations of Cu in M. albus as compared to Oreochromis spp. Cadmium (Cd), is a nonessential element that can produce severe adverse effects by decreasing the survival rate, growth and reproduction of aquatic organisms when present at toxic concentrations (Sorensen 1991; Hilmy et al. 1985). The Malaysian Food Regulation (1985) set a permissible limit for Cd at 1 lg/g wet weight. Resuspension of soil particles as a result of plowing activities may have increased metal concentrations in the paddy field areas (Sow et al. 2012b). Increased amounts of these metals could then be available for accumulation into organisms. Another factor that may have influenced the observed difference between the two species is their contact with the sediment. The eel, M. albus may spend more time in contact with the sediment than Oreochromis spp. For the three plowing stages, significant positive correlations (p \ 0.05) were obtained between metal concentrations in liver and muscles tissue in all cases, and between sediment and either liver or muscle tissue in most cases (Table 3). An exception was the association between metal concentrations in sediment and muscle tissue in May.

Bull Environ Contam Toxicol Table 3 Pearson’s correlation coefficient (r) for metal concentrations in liver, muscle and sediment during different plowing stages Month

Liver

Muscle

Sediment

Liver

1

0.808**

0.464**

Muscle

0.808**

1

0.392**

Sediment

0.464**

0.392**

1

Table 4 Biota-sediment accumulation factor (BSAF) for metals in liver and muscle of M. albus from a paddy field in Tumpat, Malaysia during different plowing stages Sample

March

April

May

Plowing stage

BSAF Cu

Liver

Zn

Cd

Ni

1

0.23b

1.48b

1.11b

1.12a

a

a

2.09

8.73

a

0.45b

Liver

1

0.908**

0.611**

2

0.34

Muscle

0.908**

1

0.496**

3

0.22b

2.17a

2.81a

0.01b

Sediment

0.611**

0.496**

1

Mean

0.26

1.91

4.22

0.53

Liver Muscle

1 0.815**

0.815** 1

0.39* 0.24

1

0.03a

0.93ab

1.00b

0.96a

2

0.04

a

2.12

a

0.14b

3

0.01

b

0.65

0.49

b

0.01b

Mean

0.03

0.91

1.2

Sediment

0.39*

0.24

1

* Correlation is significant at the level 0.05 (2-tailed) ** Correlation is significant at the level 0.01 (2-tailed)

During the plowing activity, the long-term accumulated heavy metals in paddy soil may be resuspended on the surface paddy soil. Similar event has been reported by Zulkifli et al. (2010a) for disturbed sediments. Natural or human mediated activities can disturb soil layers, which may expose the underneath contaminated layers. Resuspended sediment-bound pollutants may be taken up by aquatic organisms. Since eels are long-lived, the longer exposure period of swamp eels to heavy metals may allow them to accumulate high concentrations of pollutants in their body tissues. Therefore, even sediment and water with lower concentrations of pollutants could be potentially harmful (Brusle´ 1989). Monopterus albus is commercially important, as it is widely consumed by local residents. Razak et al. (2001) reported that the muscle of M. albus contains a high content of lipid (0.50–1.06 g/100 g muscle tissue) and significant amounts of fatty acids, including palmitic (10.8/100 g lipid), oleic (8.54/100 g lipid), arachidonic (8.25/100 g lipid) and docosahexaenoic (6.21/100 g lipid). According to Kargin and Erdem (1991), muscle tissue of freshwater fish usually is not considered as a metal accumulator. In this study, muscle tissue of M. albus was found to bioaccumulate low concentrations of metals during the plowing season. Significantly low concentrations of Cu may reflect low amounts of binding proteins in the muscle (Allen-Gil and Martynov 1995). Cu and Zn are essential elements and are carefully regulated by physiological mechanisms in most organisms (Eisler 1988). Based on Malaysian Food Regulation (1985), the permissible limits recommended for Cd, Cu and Zn are 1, 30 and 100 lg/g wet weight, respectively. For a general comparison to these permissible limits, the dry weight metal concentrations may be divided by 5 to obtain an approximation of wet weight concentrations. The resultant estimates of mean metal concentrations on a wet

Muscle

a

1.15

b

0.37

Post-hoc: Mean BSAF values for liver and muscle sharing a common letter for a particular metal are not significantly different, p [ 0.05

weight basis for Cd, Cu and Zn in muscle tissue would be 0.24, 0.13 and 9.76 lg/g wet weight respectively. These would all be well within the safety range. Similarly, this would also be the case for liver tissue. Ni showed a generally low toxicity as reported by Khangarot and Ray (1990), but can cause sublethal effects to aquatic organisms when the concentrations are increased. The accumulation of Ni in freshwater fish ranged from 10 to 120 lg/g (Tong 1974; Vos and Hovens 1986). In the case of Ni, the permissible limit proposed by the Food and Drug Administration (2001) was 70–80 lg/g wet weight for crustaceans, clam, oysters and mussels. The mean concentrations of Ni in both tissues were well below the permissible limits. These guidelines showed muscle and liver parts of M. albus are safe for consumption. Arnot and Gobas (2006) stated the importance of assessing the degree of accumulation of pollutants in organisms based on both dietary intake and uptake from the ambient environment. In the present study, significantly greater (p \ 0.05) BSAF values were observed for liver as compared to muscle tissue (Table 4). In liver, the BSAF values was significantly different between Stage 1 and other stages (Stage 2 and 3) for liver and muscle (p \ 0.05). As for muscle, the BSAF values were significantly different between stage 3 and the other stages (p \ 0.05). Different bioaccumulation rates of metals are partially influenced by content of metallothioneins in the tissues. Canli and Atli (2003) reported that metallothioneins, which are metalbinding proteins, play a vital role in the differences of metal concentrations in the tissues. Also, metabolic organs, particularly the liver, have the ability to detoxify metals by producing metallothioneins (Karadede et al. 2004). Canli and Atli (2003) found that fish liver and gill tissues accumulated the highest concentrations of metals.

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In conclusion, this study has shown that Cd, Cu, Zn and Ni are accumulated in tissues of M. albus collected from rice paddy fields. However, measured metal concentrations in the edible muscle tissue were within the safety ranges established by governmental agencies, indicating that M. albus is safe to be eaten by local residents. Acknowledgments This study was jointly supported by the Research University Grant Scheme, RUGS (03-01-11-1155RU) awarded by Universiti Putra Malaysia, the Fundamental Research Grant Scheme, FRGS (Project No.: FRGS/1/11/ST/UPM/02/12) and the Exploratory Research Grant Scheme, ERGS (Project No.: ERGS/1-2012/5527109) awarded by the Ministry of Higher Education, Malaysia.

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