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Trace Metal and Organochlorine Residue Levels in Red Mullet (Mullus barbatus) from the Eastern Aegean, Turkey
PII: S0043-1354(00)00504-2
Wat. Res. Vol. 35, No. 9, pp. 2327–2332, 2001 # 2001 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0043-1354/01/$ - see front matter
RESEARCH NOTE TRACE METAL AND ORGANOCHLORINE RESIDUE LEVELS IN RED MULLET (MULLUS BARBATUS ) FROM THE EASTERN AEGEAN, TURKEY F. KUCUKSEZGIN*, O. ALTAY, E. ULUTURHAN and A. KONTAS Institute of Marine Sciences & Technology, Dokuz Eylul University, Inciralti, 35340 Izmir, Turkey (First received 26 January 2000; accepted in revised form 10 October 2000) Abstract}The levels of trace metals and organochlorine residue were determined in red mullet (Mullus barbatus) in the framework of a MED-POL II Project for the Aegean Sea during 1994–1998. Samples were analyzed seasonally from July 1994 to January 1998. The concentrations of trace metals found varied with Hg: 16–200 mg kg1, Cd: 0.57–4.5 mg kg1 and Pb: 40–207 mg kg1 wet weight. The order of trace metal concentrations found in Mullus barbatus was Pb>Hg>Cd. Correlation coefficients were calculated between Hg, Cd, and Pb concentrations and fork lengths to be Hg: 0.5852, Cd: 0.081, Pb: 0.5823, respectively. Cadmium levels are lower than the results in fish tissues reported from Mediterranean regions. The results of organochlorine residues measured varied between Aldrin: 0.10 and 0.61 mg kg1, t-DDD: 0.86 and 4.5 mg kg1 and t-DDE: 10 and 18 mg kg1 wet weight. Correlation coefficients for measured organochlorine residues and fork lengths are Aldrin: 0.6422, t-DDD: 0.2237 and t-DDE: 0.5484. The levels of mercury, lead and organochlorine residues are similar to the results in fish from Mediterranean countries. # 2001 Elsevier Science Ltd. All rights reserved Key words}fish, trace metals, organochlorine residue, bioaccumulation, toxicity, Aegean Sea
INTRODUCTION
The Aegean Sea is one of the Eastern Mediterranean subbasins located between the Greek and Turkish coasts (2833 km) and islands of Crete and Rhodes. The study area extends from Saros Bay in the north to Fethiye in the southeastern Aegean. Trace contaminants are important constituents of aquatic ecosystems. Heavy metal contamination of the environment has been recognized as a serious pollution problem. The variability in metal concentrations of marine organisms depends on many factors, either environmental, or purely biological (Phillips, 1995). Fish are widely used as sentinels of contamination in aquatic environment. The levels of metals accumulated in some marine organisms may be many orders of magnitude above background of certain species as bioindicators of heavy metal pollution (Pastor et al., 1994, 1996). In particular, mercury has received much attention due to the wellknown toxic effects of this metal. Among a large number of man-made chemicals, organochlorines such as Aldrin, DDD, DDE and PCBs are of great concern due to their highly
*Author to whom all correspondence should be addressed. Tel.: +90-232-278-55-65; fax: +90-232-278-50-82; e-mail: [email protected]
bioaccumulative nature and toxic biological effects. These chemicals are persistent in nature, biomagnify in the food web and impose various toxic effects in marine organisms (Tanabe et al., 1997). In the last few years, increasing attention has been paid to the relationship between the conformation of organochlorines and their impact on marine and terrestrial biota (Duinker et al., 1991; Ahlborg et al., 1994; Hu¨hnerfuss et al., 1995). The present environmental problems are due to unmanaged shipping activity, river run-off (Gediz is the biggest river along the eastern Aegean), untreated sewage discharge by coastal settlements, dumping of toxic and industrial wastes from the western part of Turkey. Monitoring of mercury, cadmium, lead and organochlorines levels in red mullet (Mullus barbatus) was conducted in the eastern Aegean during 1994–1998 in the framework of a MEDPOL II Project for the Aegean Sea. Red mullets, being bottom dwellers to a certain extent, are species that tend to concentrate contaminants to a higher degree than other species due to high mobility. For this reason it was recommended by FAO/UNEP (1993) as monitoring species. A number of studies have determined the trace metal concentrations in the western Aegean and western, eastern and central Mediterranean Sea (Vasilikiotis et al., 1983; Hornung and Kress, 1991; Barghigiani and De Ranieri, 1992;
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Bei et al., 1992; Pastor et al., 1994). Of all the research on the concentrations of trace metals in the eastern Aegean environment only a little has been carried out (Kucuksezgin and Balci, 1994; MED-POL, 1995, 1997), but no published data are available on organochlorine concentrations in the Eastern Aegean except technical reports of MEDPOL projects. In this paper, the levels of Hg, Cd, Pb and organochlorine residues in Mullus barbatus from Eastern Aegean shores are presented and compared during different seasons. Furthermore, the present study discusses the relationship between trace metals, organochlorine levels and fork lengths.
MATERIAL AND METHODS
A number of sampling stations were sampled as part of six cruises of the R/V K. Piri Reis to this area in 1994, 1995, 1996, 1997 and 1998. The locations of stations are given in Fig. 1. Biota samples were collected by trawling from sampling stations, placed in plastic bags and stored at below 208C until trace metal analysis. Fork length and the fresh weight of fish samples were recorded prior to the dissection. Samples were dissected according to UNEP (1984). Homogenize the fillets in a blender and approximately 5–7 g of homogenate (muscle) was digested with 5 : 1 HNO3 : HClO4 in microwave digestion system and diluted to the desired volume with double distilled water (UNEP, 1982, 1984, 1985). All the analyses were performed by Varian atomic absorption spectrophotometer. Total mercury concentration was measured by cold vapor technique and Cd, Pb were determined by graphite furnace and background corrections were used as required. The detection limits for trace metals were Hg: 0.05, Cd: 0.10 and Pb: 0.10 mg l1. Intercalibration fish homogenate (MA-MEDPOL-1/TM) sample (from the International Laboratory of Marine Radioactivity, IAEA, Monaco) was used as a control for the analytical methods. The values obtained (in mg g1 dry wt) for the
analysis of six replicates of this sample were as follows: Hg (certified 2.69 0.17; found 2.77; S.D. : 0.04), Cd (certified 0.015 0.012; found 0.018, S.D. : 0.02), Pb (certified 0.074 0.015; found 0.064; S.D. : 0.02). Biota samples were handled carefully to reduce external contamination, placed individually on and wrapped in several layers of aluminium foil and stored at below 208C until organochlorine analysis (UNEP, 1991). All samples were thawed and fork lengths were measured. After dissection of the samples, fillets were homogenized to prepare a composite sample. About 15 g of samples were homogenized with anhydrous Na2SO4 (1 : 3) supplying a powder that was extracted in a soxhlet apparatus for 8 h with 250 ml n-hexane of analytical grade. The extract was concentrated to 10 ml by rotary evaporator and higher molecular lipids were separated by means of concentrated sulphuric acid of analytical-reagent grade (‘H2SO4 clean up’). Sample extracts were fractionated by alumina/silica (70–230 mesh ASTM) column chromatography. The alumina was activated at 4008C for 4 h and partially deactivated with 1% distilled water (v/w). The silica was activated at 1708C for 12 h and deactivated partially with 5% distilled water (v/w) (method described in UNEP, 1982b). The column was sequentially eluted with 60 ml of nhexane (aldrin, heptachlor, DDE, DDT, PCBs fraction) and 50 ml of diethylether : n-hexane (1 : 9 v/v), 25 ml of diethylether : n-hexane (2 : 8 v/v) (endosulphan, dieldrin, lindane, o,p-DDD, p , p-DDD, endrin fraction). The extracts were concentrated to 1 ml in n-hexane. Approximately 1 ml of each extract was injected in the splitless mode onto gas chromatography. Gas chromatography analyses were carried out using a Chrompack and an electron capture detector (ECD;63Ni, temperature: 2508C) with a CP Sil 19CB fused silica capillary column (Chrompack; 30 m 0.32 mm i.d.; film thickness 0.2 mm). The oven temperature was programmed from 120 (1 min) to 2508C at a rate of 38C min1, with the injector temperature set at 2408C. The carrier gas was nitrogen. Identification of organochlorines was based on comparison of the measured retention times with those of known standards. Organochlorines were quantified by comparing the areas of each peak with the area of the internal standard (methoxychlor). Individual response factors were calculated for each organochlorine to correct the measured areas. Blanks of pure n-hexane were periodically run to ensure the purity of the system. Recovery standards were added to the samples before extraction. The average recoveries were as follows: aldrin 96%, lindane 94%, hepthachlor 98%, DDE 80%, DDTs 95%, endosulfan 87%, dieldrin 89%, endrin 88%, tDDD 99% and HCB 97% (results were not corrected for recovery). The detection limits for organochlorines and PCB (Aroclor-1254) were 0.10 and 3.0 ng g1 on a wet weight basis, respectively. Intercalibration sample (IAEA-408, from IAEA, Monaco) was used as a control for the analytical methods. The results obtained (in ng g1 dry wt) for the analysis of six replicates of this sample were as follows: pp-DDE (certified 1.4 0.63; found 0.90; S.D. : 0.047), pp-DDD (certified 1.1 0.74; found 1.7; S.D. : 0.028). RESULTS AND DISCUSSION
Trace metals The results of the metal analysis in the muscle tissue, the range of fork length and weight are summarized in Table 1 for each sampling area.
Fig. 1. Location of stations in the Aegean Sea.
Mercury. The concentration levels of mercury found in Mullus barbatus range from 16 to 200 mg kg1 (wet wt.) in the eastern Aegean (Table 2). The results obtained in the Mediterranean Sea
Trace metal and organochlorine residue levels in red mullet
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Table 1. Trace metal concentrations in Mullus barbatus (mg kg1 wet weight) Sampling date/station Summer 1994 1 2 3 4 5 7 8 9 Spring 1995 2 3 4 5 6 7 8 9 Summer 1996 2 4 5 6 8 9 10 12 Fall 1996 1 3 6 8 9 10 Fall 1997 2 4 5 7 7 8 9 10 10 Winter 1998 2 3 3 4 4 5 5 8 8 9 10 11 12
No. of individuals
Range of fork length (mm)
4 10 5 10 10 10 5 10
118–138 140–180 110–125 140–160 110–145 108–142 134–145 106–115
10 10 10 12 10 10 10 10
Hg
Cd
Pb
26–39 48–63 25–38 50–65 25–36 25–37 29–40 21–25
51 98 30 120 71 87 52 23
3.8 4.1 3.9 3.2 2.9 3.1 1.9 1.9
138 139 119 146 179 116 110 122
120–135 124–138 128–145 130–155 111–145 120–145 130–148 128–145
27–41 28–44 28–40 28–65 20–38 26–40 28–40 27–39
62 16 18 21 66 27 21 19
3.1 1.8 1.2 3.1 1.3 1.7 2.5 2.3
108 115 150 152 146 109 110 113
10 10 9 10 10 8 10 10
130–145 128–145 134–150 120–140 132–156 135–160 125–137 132–160
26–38 29–41 33–60 27–35 30–65 36–66 28–42 33–59
95 84 104 84 38 74 44 72
3.6 2.1 2.3 3.2 4.1 2.2 2.1 2.3
129 138 124 127 110 158 124 118
11 10 24 20 20 15
110–150 120–135 155–200 130–160 140–180 143–165
22–58 28–41 58–96 31–61 39–92 54–88
69 92 190 114 146 160
1.9 2.9 2.1 3.2 3.8 3.3
128 113 135 85 153 112
5 7 10 5 20 4 6 20 7
160–185 110–138 130–148 170–190 140–170 141–169 120–165 110–120 145–165
65–108 30–38 33–48 78–103 40–75 39–78 26–72 21–28 55–67
200 70 87 116 103 129 134 37 97
3.2 3.4 1.4 1.3 0.63 3.0 4.3 3.2 1.5
175 40 110 187 99 124 120 115 133
10 10 10 6 10 4 10 10 9 5 9 10 10
124–135 140–162 124–138 150–163 125–133 186–194 150–170 115–135 137–144 162–182 123–140 135–145 112–130
28–36 46–68 26–38 48–70 28–36 104–126 50–80 24–44 38–48 72–98 34–48 10–20 24–32
137 141 95 122 92 183 110 118 136 133 135 141 40
1.4 2.4 1.2 0.57 1.1 4.5 1.1 4.3 2.4 1.4 0.79 1.5 3.9
108 165 149 180 137 207 95 77 72 196 135 80 41
agree with this work (Hornung and Kress, 1991; Giordano et al., 1991; Pastor et al., 1994; Focardi et al., 1998). In general the mercury values obtained are lower than Tyrrhenian and Adriatic Sea (Sapunar et al., 1989; Rossi et al., 1993). Mercury concentration increases with increasing size of the sample and the accumulation is associated with its food and feeding habits. It is known that the position of the fish in food chain is an important factor determining its mercury content (Bernhard, 1988). The relationship between mercury concentration and fork length was significant ( y ¼ 86:716 þ 1:389x, R ¼ 0:5852).
Range of weight (g)
Mercury concentration points out a significant variation as a function of the sampling periods. Samples collected during the warm period of the year, especially during spring, summer when their gonads were well developed (Benli et al., 1996), muscle tissue showed lower mercury concentrations. This fact is probably related to the fish’s biological cycle. Total lipid contents increase in muscle tissue during cold period and high levels of mercury were observed in winter. Maximum concentrations of mercury permitted in marine organisms are similar in the majority of
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Mediterranean countries, ranging between 500 and 700 mg kg1 (FAO, 1984). The maximum value of mercury 200 mg kg1 indicated for the edible parts of fish. The consumption of 1500 g per week of this fish in the human diet would represent the maximum tolerable consumption of mercury (300 mg mercury per week per 60 kg man).
Cadmium. Cadmium concentrations found varied from 0.57 to 4.5 mg kg1 (wet wt.) in the eastern Aegean Sea (Table 2). The mean concentrations of cadmium were lower than the levels in fish tissues reported from Mediterranean regions (TaliadouriVoutsinou, 1982; UNEP, 1989; Giordiano et al., 1991; Bei et al., 1992). Cadmium in fish muscle is generally less than 0.1 mg g1 (dry wt), although fish in contaminated environments may have levels of one-to-two orders of magnitude higher (Pastor et al., 1994). Cadmium concentrations in muscle tissue showed no relation to fork length (R ¼ 0:0808). No significant variations were observed for different seasons. The provisionally tolerable weekly intake was estimated by FAO/WHO expert committee at 400–500 mg cadmium per person per week (UNEP, 1989). The maximum value of cadmium is 4.5 mg kg1
in the sampling area. A person can consume more than 300 meal of fish per week. Lead. Concentrations of lead were in the range 40–207 mg kg1 (wet wt) (Table 2). The results agree with Giordano et al. (1991), Pastor et al. (1994), Storelli et al. (1998) and generally lower than the limit of 2.0 mg kg1 wet weight established by European countries (UNEP, 1985). The lead concentrations increase with the increasing fork length in Mullus barbatus (y ¼ 86:549þ 1:457x, R ¼ 0:5823). There have been no significant differences in the values among the various sampling periods (Table 1). Maximum concentration of lead 207 mg kg1 was observed for the muscle of fish. A person can consume 48 meals per week of this fish in the human diet which would represent the tolerable weekly intake of lead (3000 mg lead per 60 kg man) according to the UNEP (1985). Organochlorine residues The concentrations of organochlorine residues in the eastern Aegean Sea are shown in Table 3. The composition of DDT and its metabolites was generally in the order of p; p0 -DDE (46%), p; p0 -DDD
Table 2. Mean concentrations of trace metals and organochlorine residues in Mullus barbatus, their associated standard deviations, maximum and minimum values observed with 95% confidence intervals. Concentrations are expressed in mg kg1 wet weight
No.of sample Mean Min. Max. S.D.
Hg
Cd
Pb
Aldrin
t-DDD
t-DDE
52 90.56 16 200 47.37
52 2.49 0.57 4.5 1.07
52 126.36 40 207 33.84
18 0.26 0.10 0.61 0.14
18 1.94 0.86 4.5 0.97
18 14.44 10 18 2.48
Table 3. Sample numbers, biological data and organochlorine residues in Mullus barbatus (mg kg1) Location
May 1995 2 3 4 5 6 7 8 9 Sept.1995 2 3 5 5 6 6 7 7 8 9
No of indiv.
Mean FL (mm)
Lipids (%)
Concentration (wet wt. basis)
Concentration (lipid wt. basis)
Aldrin
t-DDD
t-DDE
Aldrin
t-DDD
t-DDE
10 10 10 10 10 10 9 10
148 130 137 145 129 133 139 140
1.4 1.3 1.3 1.4 1.2 1.3 1.3 1.4
0.15 0.10 0.29 0.10 0.15 0.28 0.20 0.10
2.7 1.7 1.6 0.86 1.0 1.2 2.4 0.90
11 13 10 13 14 12 15 12
11.1 7.7 21.0 7.3 11.7 21.3 15.4 7.4
200 131 118 63.0 78.0 91.0 185 66.0
815 1000 741 954 1088 914 1155 892
7 20 10 10 10 10 20 20 10 20
150 130 145 136 170 145 175 145 168 135
5.1 4.2 4.2 5.6 6.0 5.6 6.5 5.4 5.8 4.5
0.25 0.15 0.18 0.42 0.39 0.61 0.44 0.35 0.29 0.20
3.2 4.5 1.1 1.2 1.8 1.5 2.6 2.0 3.0 1.6
16 15 15 12 18 15 18 17 18 16
4.9 3.6 4.3 7.5 6.5 11.0 6.7 6.5 5.0 4.4
63.0 107 26.2 21.4 30.0 27.0 40.0 37.0 52.0 36.0
315 357 357 214 300 268 276 315 309 356
Trace metal and organochlorine residue levels in red mullet
(34%), p; p0 -DDT (16%) and o; p0 -DDT (4%) (Tanabe et al., 1997). In Turkey, the organochlorine insecticides were used in quantities of 1000–2000 t annually between 1976 and 1983 (Karakaya and Ozalp, 1987). It is suggested that some organochlorines in particular DDT have not been used in recent years in the watershed of the eastern Aegean Sea. Concentrations of DDE and DDD ranged between 10–18 and 0.86–4.5 mg kg1 (wet wt.), respectively, in Mullus barbatus. The levels of Aldrin varied between 0.10 and 0.61 mg kg1 in samples in the eastern Aegean Sea (Table 2). Lipid content (HEOM: the extractable organic matter with hexane) determined with the aid of soxhlet extraction of samples with hexane, was found to be 1.2–1.4%, 4.2–6.5% in May and September, respectively. The samples were collected during and after spawning season, as it is known that feeding intensity and consequently lipid concentrations and pollutant body burdens decrease in fish during the spawning activity (Benli et al., 1996; Pastor et al., 1996). Fish lipid content can substantially influence the bioaccumulation of organochlorinated compounds. A positive relationship was apparent between lipid content and organochlorine concentrations during sampling periods. This relationship between organochlorine accumulation and lipids has been reported in various studies concerning Mullus barbatus (Satsmadjis et al., 1988a; Vassilopoulou and Georgekopoulos-Gregorides, 1993; Giouranovits-Psyllidou et al., 1994). Fish size (age) is also known to play a role in pollutant accumulation, organochlorine concentrations generally increases as fish grow (Larsson et al., 1991; Giouranovits-Psyllidou et al., 1994). This observation was also consistent with our results; correlation coefficients were calculated for Aldrin (R ¼ 0:6422), t-DDE (R ¼ 0:5484), t-DDD (R ¼ 0:2237). Other organochlorinated compounds (o; p0 -DDT, p; p0 DDT, heptachlor, endosulphan, dieldrin, lindane, endrin) were below the detection limit of 0.10 mg kg1 wet weight. The organochlorine values presented in this study are close to the results in fish tissues reported by Georgekopoulos-Gregorides et al. (1991) and Giouranovits-Psyllidou et al. (1994), collected at the different parts of the Aegean Sea. Tanabe et al. (1997) reported higher concentration of organochlorine residues (resulting from organic waste pollution through the rivers) in fish from Black Sea compared to this study. PCBs were not detected in Mullus barbatus analyzed in our experimental conditions. This observation is consistent with results reported by Elder and Villeneuve (1977), Basturk et al. (1980), Salihoglu et al. (1980). They observed a decreasing trend in the PCB concentrations from the western towards the eastern Mediterranean. Harvey et al. (1974a) and Bidelman and Olney (1974) explained low dissolved PCB values in the Sargasso Sea by a co-distillation process and Phillips (1995) explained organochlorine
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compounds are subject to co-distillation processes (despite their low vapor pressure) and are therefore transported globally through the atmosphere. In the eastern Mediterranean evaporation also exceeds precipitation and co-distillation of PCBs is also possible in the Aegean Sea.
CONCLUSIONS
In conclusion, we have carried out analyses on the levels of trace metals in the muscle tissue of Mullus barbatus from the eastern Aegean Sea. Mercury and lead concentrations are similar to those reported in fish from Mediterranean countries. Cadmium levels are lower than the results in fish tissues reported from Mediterranean regions. Some generalizations can be inferred from the mean trace metal levels in fish. The order of the metal concentrations found in Mullus barbatus was Pb>Hg>Cd. It is apparent from the above discussions that the period of exposure (age) is a governing parameter in pollutant uptake, but also that the lipid content and the dietary intake influence body burdens. The results cannot be totally explained without taking into account physiological processes and primarily tissue growth and metabolism. These may also play a dominant role in limiting chemical accumulation. Data reported here demonstrate that Mullus barbatus exhibit increase of organochlorine concentrations with fish size (age) and lipid content. REFERENCES
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Wat. Res. Vol. 35, No. 9, pp. 2327–2332, 2001 # 2001 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0043-1354/01/$ - see front matter
RESEARCH NOTE TRACE METAL AND ORGANOCHLORINE RESIDUE LEVELS IN RED MULLET (MULLUS BARBATUS ) FROM THE EASTERN AEGEAN, TURKEY F. KUCUKSEZGIN*, O. ALTAY, E. ULUTURHAN and A. KONTAS Institute of Marine Sciences & Technology, Dokuz Eylul University, Inciralti, 35340 Izmir, Turkey (First received 26 January 2000; accepted in revised form 10 October 2000) Abstract}The levels of trace metals and organochlorine residue were determined in red mullet (Mullus barbatus) in the framework of a MED-POL II Project for the Aegean Sea during 1994–1998. Samples were analyzed seasonally from July 1994 to January 1998. The concentrations of trace metals found varied with Hg: 16–200 mg kg1, Cd: 0.57–4.5 mg kg1 and Pb: 40–207 mg kg1 wet weight. The order of trace metal concentrations found in Mullus barbatus was Pb>Hg>Cd. Correlation coefficients were calculated between Hg, Cd, and Pb concentrations and fork lengths to be Hg: 0.5852, Cd: 0.081, Pb: 0.5823, respectively. Cadmium levels are lower than the results in fish tissues reported from Mediterranean regions. The results of organochlorine residues measured varied between Aldrin: 0.10 and 0.61 mg kg1, t-DDD: 0.86 and 4.5 mg kg1 and t-DDE: 10 and 18 mg kg1 wet weight. Correlation coefficients for measured organochlorine residues and fork lengths are Aldrin: 0.6422, t-DDD: 0.2237 and t-DDE: 0.5484. The levels of mercury, lead and organochlorine residues are similar to the results in fish from Mediterranean countries. # 2001 Elsevier Science Ltd. All rights reserved Key words}fish, trace metals, organochlorine residue, bioaccumulation, toxicity, Aegean Sea
INTRODUCTION
The Aegean Sea is one of the Eastern Mediterranean subbasins located between the Greek and Turkish coasts (2833 km) and islands of Crete and Rhodes. The study area extends from Saros Bay in the north to Fethiye in the southeastern Aegean. Trace contaminants are important constituents of aquatic ecosystems. Heavy metal contamination of the environment has been recognized as a serious pollution problem. The variability in metal concentrations of marine organisms depends on many factors, either environmental, or purely biological (Phillips, 1995). Fish are widely used as sentinels of contamination in aquatic environment. The levels of metals accumulated in some marine organisms may be many orders of magnitude above background of certain species as bioindicators of heavy metal pollution (Pastor et al., 1994, 1996). In particular, mercury has received much attention due to the wellknown toxic effects of this metal. Among a large number of man-made chemicals, organochlorines such as Aldrin, DDD, DDE and PCBs are of great concern due to their highly
*Author to whom all correspondence should be addressed. Tel.: +90-232-278-55-65; fax: +90-232-278-50-82; e-mail: [email protected]
bioaccumulative nature and toxic biological effects. These chemicals are persistent in nature, biomagnify in the food web and impose various toxic effects in marine organisms (Tanabe et al., 1997). In the last few years, increasing attention has been paid to the relationship between the conformation of organochlorines and their impact on marine and terrestrial biota (Duinker et al., 1991; Ahlborg et al., 1994; Hu¨hnerfuss et al., 1995). The present environmental problems are due to unmanaged shipping activity, river run-off (Gediz is the biggest river along the eastern Aegean), untreated sewage discharge by coastal settlements, dumping of toxic and industrial wastes from the western part of Turkey. Monitoring of mercury, cadmium, lead and organochlorines levels in red mullet (Mullus barbatus) was conducted in the eastern Aegean during 1994–1998 in the framework of a MEDPOL II Project for the Aegean Sea. Red mullets, being bottom dwellers to a certain extent, are species that tend to concentrate contaminants to a higher degree than other species due to high mobility. For this reason it was recommended by FAO/UNEP (1993) as monitoring species. A number of studies have determined the trace metal concentrations in the western Aegean and western, eastern and central Mediterranean Sea (Vasilikiotis et al., 1983; Hornung and Kress, 1991; Barghigiani and De Ranieri, 1992;
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Bei et al., 1992; Pastor et al., 1994). Of all the research on the concentrations of trace metals in the eastern Aegean environment only a little has been carried out (Kucuksezgin and Balci, 1994; MED-POL, 1995, 1997), but no published data are available on organochlorine concentrations in the Eastern Aegean except technical reports of MEDPOL projects. In this paper, the levels of Hg, Cd, Pb and organochlorine residues in Mullus barbatus from Eastern Aegean shores are presented and compared during different seasons. Furthermore, the present study discusses the relationship between trace metals, organochlorine levels and fork lengths.
MATERIAL AND METHODS
A number of sampling stations were sampled as part of six cruises of the R/V K. Piri Reis to this area in 1994, 1995, 1996, 1997 and 1998. The locations of stations are given in Fig. 1. Biota samples were collected by trawling from sampling stations, placed in plastic bags and stored at below 208C until trace metal analysis. Fork length and the fresh weight of fish samples were recorded prior to the dissection. Samples were dissected according to UNEP (1984). Homogenize the fillets in a blender and approximately 5–7 g of homogenate (muscle) was digested with 5 : 1 HNO3 : HClO4 in microwave digestion system and diluted to the desired volume with double distilled water (UNEP, 1982, 1984, 1985). All the analyses were performed by Varian atomic absorption spectrophotometer. Total mercury concentration was measured by cold vapor technique and Cd, Pb were determined by graphite furnace and background corrections were used as required. The detection limits for trace metals were Hg: 0.05, Cd: 0.10 and Pb: 0.10 mg l1. Intercalibration fish homogenate (MA-MEDPOL-1/TM) sample (from the International Laboratory of Marine Radioactivity, IAEA, Monaco) was used as a control for the analytical methods. The values obtained (in mg g1 dry wt) for the
analysis of six replicates of this sample were as follows: Hg (certified 2.69 0.17; found 2.77; S.D. : 0.04), Cd (certified 0.015 0.012; found 0.018, S.D. : 0.02), Pb (certified 0.074 0.015; found 0.064; S.D. : 0.02). Biota samples were handled carefully to reduce external contamination, placed individually on and wrapped in several layers of aluminium foil and stored at below 208C until organochlorine analysis (UNEP, 1991). All samples were thawed and fork lengths were measured. After dissection of the samples, fillets were homogenized to prepare a composite sample. About 15 g of samples were homogenized with anhydrous Na2SO4 (1 : 3) supplying a powder that was extracted in a soxhlet apparatus for 8 h with 250 ml n-hexane of analytical grade. The extract was concentrated to 10 ml by rotary evaporator and higher molecular lipids were separated by means of concentrated sulphuric acid of analytical-reagent grade (‘H2SO4 clean up’). Sample extracts were fractionated by alumina/silica (70–230 mesh ASTM) column chromatography. The alumina was activated at 4008C for 4 h and partially deactivated with 1% distilled water (v/w). The silica was activated at 1708C for 12 h and deactivated partially with 5% distilled water (v/w) (method described in UNEP, 1982b). The column was sequentially eluted with 60 ml of nhexane (aldrin, heptachlor, DDE, DDT, PCBs fraction) and 50 ml of diethylether : n-hexane (1 : 9 v/v), 25 ml of diethylether : n-hexane (2 : 8 v/v) (endosulphan, dieldrin, lindane, o,p-DDD, p , p-DDD, endrin fraction). The extracts were concentrated to 1 ml in n-hexane. Approximately 1 ml of each extract was injected in the splitless mode onto gas chromatography. Gas chromatography analyses were carried out using a Chrompack and an electron capture detector (ECD;63Ni, temperature: 2508C) with a CP Sil 19CB fused silica capillary column (Chrompack; 30 m 0.32 mm i.d.; film thickness 0.2 mm). The oven temperature was programmed from 120 (1 min) to 2508C at a rate of 38C min1, with the injector temperature set at 2408C. The carrier gas was nitrogen. Identification of organochlorines was based on comparison of the measured retention times with those of known standards. Organochlorines were quantified by comparing the areas of each peak with the area of the internal standard (methoxychlor). Individual response factors were calculated for each organochlorine to correct the measured areas. Blanks of pure n-hexane were periodically run to ensure the purity of the system. Recovery standards were added to the samples before extraction. The average recoveries were as follows: aldrin 96%, lindane 94%, hepthachlor 98%, DDE 80%, DDTs 95%, endosulfan 87%, dieldrin 89%, endrin 88%, tDDD 99% and HCB 97% (results were not corrected for recovery). The detection limits for organochlorines and PCB (Aroclor-1254) were 0.10 and 3.0 ng g1 on a wet weight basis, respectively. Intercalibration sample (IAEA-408, from IAEA, Monaco) was used as a control for the analytical methods. The results obtained (in ng g1 dry wt) for the analysis of six replicates of this sample were as follows: pp-DDE (certified 1.4 0.63; found 0.90; S.D. : 0.047), pp-DDD (certified 1.1 0.74; found 1.7; S.D. : 0.028). RESULTS AND DISCUSSION
Trace metals The results of the metal analysis in the muscle tissue, the range of fork length and weight are summarized in Table 1 for each sampling area.
Fig. 1. Location of stations in the Aegean Sea.
Mercury. The concentration levels of mercury found in Mullus barbatus range from 16 to 200 mg kg1 (wet wt.) in the eastern Aegean (Table 2). The results obtained in the Mediterranean Sea
Trace metal and organochlorine residue levels in red mullet
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Table 1. Trace metal concentrations in Mullus barbatus (mg kg1 wet weight) Sampling date/station Summer 1994 1 2 3 4 5 7 8 9 Spring 1995 2 3 4 5 6 7 8 9 Summer 1996 2 4 5 6 8 9 10 12 Fall 1996 1 3 6 8 9 10 Fall 1997 2 4 5 7 7 8 9 10 10 Winter 1998 2 3 3 4 4 5 5 8 8 9 10 11 12
No. of individuals
Range of fork length (mm)
4 10 5 10 10 10 5 10
118–138 140–180 110–125 140–160 110–145 108–142 134–145 106–115
10 10 10 12 10 10 10 10
Hg
Cd
Pb
26–39 48–63 25–38 50–65 25–36 25–37 29–40 21–25
51 98 30 120 71 87 52 23
3.8 4.1 3.9 3.2 2.9 3.1 1.9 1.9
138 139 119 146 179 116 110 122
120–135 124–138 128–145 130–155 111–145 120–145 130–148 128–145
27–41 28–44 28–40 28–65 20–38 26–40 28–40 27–39
62 16 18 21 66 27 21 19
3.1 1.8 1.2 3.1 1.3 1.7 2.5 2.3
108 115 150 152 146 109 110 113
10 10 9 10 10 8 10 10
130–145 128–145 134–150 120–140 132–156 135–160 125–137 132–160
26–38 29–41 33–60 27–35 30–65 36–66 28–42 33–59
95 84 104 84 38 74 44 72
3.6 2.1 2.3 3.2 4.1 2.2 2.1 2.3
129 138 124 127 110 158 124 118
11 10 24 20 20 15
110–150 120–135 155–200 130–160 140–180 143–165
22–58 28–41 58–96 31–61 39–92 54–88
69 92 190 114 146 160
1.9 2.9 2.1 3.2 3.8 3.3
128 113 135 85 153 112
5 7 10 5 20 4 6 20 7
160–185 110–138 130–148 170–190 140–170 141–169 120–165 110–120 145–165
65–108 30–38 33–48 78–103 40–75 39–78 26–72 21–28 55–67
200 70 87 116 103 129 134 37 97
3.2 3.4 1.4 1.3 0.63 3.0 4.3 3.2 1.5
175 40 110 187 99 124 120 115 133
10 10 10 6 10 4 10 10 9 5 9 10 10
124–135 140–162 124–138 150–163 125–133 186–194 150–170 115–135 137–144 162–182 123–140 135–145 112–130
28–36 46–68 26–38 48–70 28–36 104–126 50–80 24–44 38–48 72–98 34–48 10–20 24–32
137 141 95 122 92 183 110 118 136 133 135 141 40
1.4 2.4 1.2 0.57 1.1 4.5 1.1 4.3 2.4 1.4 0.79 1.5 3.9
108 165 149 180 137 207 95 77 72 196 135 80 41
agree with this work (Hornung and Kress, 1991; Giordano et al., 1991; Pastor et al., 1994; Focardi et al., 1998). In general the mercury values obtained are lower than Tyrrhenian and Adriatic Sea (Sapunar et al., 1989; Rossi et al., 1993). Mercury concentration increases with increasing size of the sample and the accumulation is associated with its food and feeding habits. It is known that the position of the fish in food chain is an important factor determining its mercury content (Bernhard, 1988). The relationship between mercury concentration and fork length was significant ( y ¼ 86:716 þ 1:389x, R ¼ 0:5852).
Range of weight (g)
Mercury concentration points out a significant variation as a function of the sampling periods. Samples collected during the warm period of the year, especially during spring, summer when their gonads were well developed (Benli et al., 1996), muscle tissue showed lower mercury concentrations. This fact is probably related to the fish’s biological cycle. Total lipid contents increase in muscle tissue during cold period and high levels of mercury were observed in winter. Maximum concentrations of mercury permitted in marine organisms are similar in the majority of
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F. Kucuksezgin et al.
Mediterranean countries, ranging between 500 and 700 mg kg1 (FAO, 1984). The maximum value of mercury 200 mg kg1 indicated for the edible parts of fish. The consumption of 1500 g per week of this fish in the human diet would represent the maximum tolerable consumption of mercury (300 mg mercury per week per 60 kg man).
Cadmium. Cadmium concentrations found varied from 0.57 to 4.5 mg kg1 (wet wt.) in the eastern Aegean Sea (Table 2). The mean concentrations of cadmium were lower than the levels in fish tissues reported from Mediterranean regions (TaliadouriVoutsinou, 1982; UNEP, 1989; Giordiano et al., 1991; Bei et al., 1992). Cadmium in fish muscle is generally less than 0.1 mg g1 (dry wt), although fish in contaminated environments may have levels of one-to-two orders of magnitude higher (Pastor et al., 1994). Cadmium concentrations in muscle tissue showed no relation to fork length (R ¼ 0:0808). No significant variations were observed for different seasons. The provisionally tolerable weekly intake was estimated by FAO/WHO expert committee at 400–500 mg cadmium per person per week (UNEP, 1989). The maximum value of cadmium is 4.5 mg kg1
in the sampling area. A person can consume more than 300 meal of fish per week. Lead. Concentrations of lead were in the range 40–207 mg kg1 (wet wt) (Table 2). The results agree with Giordano et al. (1991), Pastor et al. (1994), Storelli et al. (1998) and generally lower than the limit of 2.0 mg kg1 wet weight established by European countries (UNEP, 1985). The lead concentrations increase with the increasing fork length in Mullus barbatus (y ¼ 86:549þ 1:457x, R ¼ 0:5823). There have been no significant differences in the values among the various sampling periods (Table 1). Maximum concentration of lead 207 mg kg1 was observed for the muscle of fish. A person can consume 48 meals per week of this fish in the human diet which would represent the tolerable weekly intake of lead (3000 mg lead per 60 kg man) according to the UNEP (1985). Organochlorine residues The concentrations of organochlorine residues in the eastern Aegean Sea are shown in Table 3. The composition of DDT and its metabolites was generally in the order of p; p0 -DDE (46%), p; p0 -DDD
Table 2. Mean concentrations of trace metals and organochlorine residues in Mullus barbatus, their associated standard deviations, maximum and minimum values observed with 95% confidence intervals. Concentrations are expressed in mg kg1 wet weight
No.of sample Mean Min. Max. S.D.
Hg
Cd
Pb
Aldrin
t-DDD
t-DDE
52 90.56 16 200 47.37
52 2.49 0.57 4.5 1.07
52 126.36 40 207 33.84
18 0.26 0.10 0.61 0.14
18 1.94 0.86 4.5 0.97
18 14.44 10 18 2.48
Table 3. Sample numbers, biological data and organochlorine residues in Mullus barbatus (mg kg1) Location
May 1995 2 3 4 5 6 7 8 9 Sept.1995 2 3 5 5 6 6 7 7 8 9
No of indiv.
Mean FL (mm)
Lipids (%)
Concentration (wet wt. basis)
Concentration (lipid wt. basis)
Aldrin
t-DDD
t-DDE
Aldrin
t-DDD
t-DDE
10 10 10 10 10 10 9 10
148 130 137 145 129 133 139 140
1.4 1.3 1.3 1.4 1.2 1.3 1.3 1.4
0.15 0.10 0.29 0.10 0.15 0.28 0.20 0.10
2.7 1.7 1.6 0.86 1.0 1.2 2.4 0.90
11 13 10 13 14 12 15 12
11.1 7.7 21.0 7.3 11.7 21.3 15.4 7.4
200 131 118 63.0 78.0 91.0 185 66.0
815 1000 741 954 1088 914 1155 892
7 20 10 10 10 10 20 20 10 20
150 130 145 136 170 145 175 145 168 135
5.1 4.2 4.2 5.6 6.0 5.6 6.5 5.4 5.8 4.5
0.25 0.15 0.18 0.42 0.39 0.61 0.44 0.35 0.29 0.20
3.2 4.5 1.1 1.2 1.8 1.5 2.6 2.0 3.0 1.6
16 15 15 12 18 15 18 17 18 16
4.9 3.6 4.3 7.5 6.5 11.0 6.7 6.5 5.0 4.4
63.0 107 26.2 21.4 30.0 27.0 40.0 37.0 52.0 36.0
315 357 357 214 300 268 276 315 309 356
Trace metal and organochlorine residue levels in red mullet
(34%), p; p0 -DDT (16%) and o; p0 -DDT (4%) (Tanabe et al., 1997). In Turkey, the organochlorine insecticides were used in quantities of 1000–2000 t annually between 1976 and 1983 (Karakaya and Ozalp, 1987). It is suggested that some organochlorines in particular DDT have not been used in recent years in the watershed of the eastern Aegean Sea. Concentrations of DDE and DDD ranged between 10–18 and 0.86–4.5 mg kg1 (wet wt.), respectively, in Mullus barbatus. The levels of Aldrin varied between 0.10 and 0.61 mg kg1 in samples in the eastern Aegean Sea (Table 2). Lipid content (HEOM: the extractable organic matter with hexane) determined with the aid of soxhlet extraction of samples with hexane, was found to be 1.2–1.4%, 4.2–6.5% in May and September, respectively. The samples were collected during and after spawning season, as it is known that feeding intensity and consequently lipid concentrations and pollutant body burdens decrease in fish during the spawning activity (Benli et al., 1996; Pastor et al., 1996). Fish lipid content can substantially influence the bioaccumulation of organochlorinated compounds. A positive relationship was apparent between lipid content and organochlorine concentrations during sampling periods. This relationship between organochlorine accumulation and lipids has been reported in various studies concerning Mullus barbatus (Satsmadjis et al., 1988a; Vassilopoulou and Georgekopoulos-Gregorides, 1993; Giouranovits-Psyllidou et al., 1994). Fish size (age) is also known to play a role in pollutant accumulation, organochlorine concentrations generally increases as fish grow (Larsson et al., 1991; Giouranovits-Psyllidou et al., 1994). This observation was also consistent with our results; correlation coefficients were calculated for Aldrin (R ¼ 0:6422), t-DDE (R ¼ 0:5484), t-DDD (R ¼ 0:2237). Other organochlorinated compounds (o; p0 -DDT, p; p0 DDT, heptachlor, endosulphan, dieldrin, lindane, endrin) were below the detection limit of 0.10 mg kg1 wet weight. The organochlorine values presented in this study are close to the results in fish tissues reported by Georgekopoulos-Gregorides et al. (1991) and Giouranovits-Psyllidou et al. (1994), collected at the different parts of the Aegean Sea. Tanabe et al. (1997) reported higher concentration of organochlorine residues (resulting from organic waste pollution through the rivers) in fish from Black Sea compared to this study. PCBs were not detected in Mullus barbatus analyzed in our experimental conditions. This observation is consistent with results reported by Elder and Villeneuve (1977), Basturk et al. (1980), Salihoglu et al. (1980). They observed a decreasing trend in the PCB concentrations from the western towards the eastern Mediterranean. Harvey et al. (1974a) and Bidelman and Olney (1974) explained low dissolved PCB values in the Sargasso Sea by a co-distillation process and Phillips (1995) explained organochlorine
2331
compounds are subject to co-distillation processes (despite their low vapor pressure) and are therefore transported globally through the atmosphere. In the eastern Mediterranean evaporation also exceeds precipitation and co-distillation of PCBs is also possible in the Aegean Sea.
CONCLUSIONS
In conclusion, we have carried out analyses on the levels of trace metals in the muscle tissue of Mullus barbatus from the eastern Aegean Sea. Mercury and lead concentrations are similar to those reported in fish from Mediterranean countries. Cadmium levels are lower than the results in fish tissues reported from Mediterranean regions. Some generalizations can be inferred from the mean trace metal levels in fish. The order of the metal concentrations found in Mullus barbatus was Pb>Hg>Cd. It is apparent from the above discussions that the period of exposure (age) is a governing parameter in pollutant uptake, but also that the lipid content and the dietary intake influence body burdens. The results cannot be totally explained without taking into account physiological processes and primarily tissue growth and metabolism. These may also play a dominant role in limiting chemical accumulation. Data reported here demonstrate that Mullus barbatus exhibit increase of organochlorine concentrations with fish size (age) and lipid content. REFERENCES
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