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Assessment of organotin (butyltin species) contamination in marine biota from the Eastern Aegean Sea, Turkey
Marine Pollution Bulletin 62 (2011) 1984–1988
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Assessment of organotin (butyltin species) contamination in marine biota from the Eastern Aegean Sea, Turkey F. Kucuksezgin ⇑, S. Aydin-Onen, L.T. Gonul, I. Pazi, F. Kocak Dokuz Eylul University, Institute of Marine Sciences and Technology, Inciralti, 35340 Izmir, Turkey
a r t i c l e Keywords: Butyltins Fish Mussel Barnacle TARL Eastern Aegean Sea
i n f o
a b s t r a c t The marine environment continues to be adversely affected by tributyltin (TBT) release from maritime traffic. Therefore the concentrations of TBT, dibutyltin (DBT) and monobutyltin (MBT) were measured in barnacles, mussels and fish along the Eastern Aegean coastline. The average concentrations of TBT ng Sn g1 were found to be 235 in fish, 116 in mussels and 635 in barnacles. The highest concentrations of TBT, DBT and MBT were observed in the barnacles which had been sampled in marinas and harbors. All mussels sampled showed values of TBT + DBT, which were below the ‘‘tolerable average residue level (TARL)’’ as currently accepted. This indicates a lack of risk to the consumer. However, 7 out of the 15 fish sampled displayed TBT + DBT levels above the TARL, which indicates that a fish consumer group may be at risk. Barnacles have high potential as biomonitors for the presence of organotin in the Aegean Sea. Ó 2011 Elsevier Ltd. All rights reserved.
Since the early 1960s organotin compounds (OTs) have been used for several purposes, such as polyvinyl chloride (PVC) stabilizers, wood preserving agents, fungicides in agricultural activities, catalysts in the production of polyurethane foams and as antifouling agents in ship paints (Fent, 1996; Wang et al., 2008). Moreover organotin compounds, due to their lipid solubility, may penetrate tissues and enter the central nervous system with great potentially toxicity to organisms (Bowen, 1988). Thus, the occurrence and the impact of organotin compounds in the environment (mostly the butyl species), in is of great concern. Due to their broad range of industrial and agrochemical applications, organotin compounds have entered a number of ecosystems in considerable amounts (Hoch, 2001). Various biological effects on non-target aquatic organisms as a result of exposure to OTs have been documented. These include reduction of growth (Salazar and Salazar, 1991); larval mortality (Tanabe et al., 2000; Zhou et al., 2003); shell thickening (Alzieu et al., 1986); low progesterone levels and delay in sexual maturation (Siah et al., 2003); imposex in gastropods, mussels, microalgae and snails (Beaumont and Newman, 1986; Zhou et al., 2003) and immunological dysfunction in fish (Zhou et al., 2003). This toxicity was related to exposure concentration and duration; to bioavailability, to the sensitivity of the organisms (Rudel, 2003) and to their bioaccumulative potential (Takahashi et al., 1999). Bivalves are the organisms most employed as biomonitors, accumulating OTs in direct proportion to environmental levels (Zhou et al., 2003; Harino et al., 2005). They are considered to be ⇑ Corresponding author. Tel.: +90 2322785565; fax: +90 2322785082. E-mail address: fi[email protected] (F. Kucuksezgin). 0025-326X/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2011.06.020
a reliable indicator of biochemical conditions in the marine environment because of their tendency to absorb and accumulate a wide range of chemicals from their surroundings (Tanabe et al., 2000). Chemicals enter bivalves through their intake of food and water and are released from them via excretion and depuration back to the water (O’Connor, 2002). Many countries worldwide have banned the application of TBTbased paints to small vessels (<25 m) and butyltins have been identified as priority hazardous substances (EU, 2001). Moreover, negotiations at the International Maritime Organization (IMO) resulted in a resolution calling for a global prohibition on the application of OT compounds in antifouling systems on ships by January 2003 and a complete prohibition by January 2008 (Rudel, 2003). Due to the ongoing legislative restrictions, various studies worldwide have shown a slow decline on TBT contamination (Hoch, 2001). Present and future restrictions will not immediately remove the TBT and its degradation products (dibutyltin and monobutyltin, DBT and MBT) from the marine environment; since these compounds are persistently retained in the sediments (Diez et al., 2002). The hot spots for TBT release in the Mediterranean are be associated with the major commercial harbors in the region (UNEP, 2002). Despite an extensive number of studies on the negative impact of TBT in marine organisms, few works exist in Europe reporting the levels of these compounds in edible fish (Shawky and Emons, 1998; Borghi and Porte, 2002; Chandrinou et al., 2006). There have been a few studies on the distribution of butyltin concentrations in Turkish coastal areas. TBT concentrations in seawater samples collected along the Turkish coast of the Mediterranean Sea have been highly variable over time and space
F. Kucuksezgin et al. / Marine Pollution Bulletin 62 (2011) 1984–1988
1985
Fig. 1. Location of sampling points.
Table 1 Results for reference material (ERM-CE477) as mg/kg dry weight. BTs
Certified value
Observed value
MBT DBT TBT
1.50 ± 0.28 1.54 ± 0.12 2.20 ± 0.19
1.57 ± 0.035 1.52 ± 0.064 1.92 ± 0.20
(bdl-33.18 ng Sn l1). The highest values have been measured in water sampled from harbors and marinas (Kubilay et al., 1996; Yemenicioglu and de Mora, 2009). This present study aims firstly to create a baseline regarding organotin levels and total tin concentrations in mussel, barnacle and fish tissues; secondly to gather more information on the use of selected species as biomonitors and finally to evaluate potential risks for BT species contamination in seafood along the Eastern Aegean coast as sampled in 2009. After reviewing the open literature on TBT toxicity Penninks (1993), derived that the TDI is 0.25 lg/kg bodyweight (bw)/day. This value is based on the observed effect of TBT on the immune function in rats. The value of 0.25 lg TBT/kg-bw/day derived by Penninks (1993) is generally accepted and referred by Kannan and Falandysz (1997), Robinson et al. (1999) and Belfroid et al. (2000). Based on the TDI of 0.25 lg/kg bw/day for TBT the maximum TDI TBT intake is 15 lg per day for a person with an average body weight of 60 kg (Kannan and Falandysz, 1997). The TARL is defined as the level in seafood that is tolerable for the average consumer with an average weight of 60 kg. This newly developed tool can be calculated according to:
TARL ¼ ðTDI 60 kg bwÞ=average daily seafood consumption
The advantage of this approach is that the TARL value can be compared directly with measured residue levels of TBT in seafood. In addition, TARL values can be the basis for appropriate authorities to derive and define the maximum residue limit (MRL) of TBT in seafood for the purposes of legislation (Belfroid et al., 2000). In the present study, different marine species (Mytilus galloprovincialis, Amphibalanus amphitrite, Mullus barbatus, Diplodus annularis, Merluccius merluccius, Solea vulgaris and Pagellus erythrinus) were sampled for BTs analysis in terms of their different feeding strategies. Samples were collected from the Saros, Candarli and Izmir Gulfs along the Eastern Aegean coast, during 2009 (Fig. 1). Izmir Gulf was represented by five sampling stations. Three of them were located in the inner part of the Gulf (Sta. 1, 2, 3), while two stations were selected (4, 5) in the outer part of the Gulf. The Gulf of Saros (Sta. 8) is located in the North Eastern Aegean Sea and has an asymmetric bathymetry with a 10 km wide shelf to the north and up to 15 km wide trough in the south. The shelf extends at a water depth of 90–120 m. Several major rivers discharge into the Saros Gulf such as Meriç River and Kavak Creek. However, there is no industry or significant settlement in the area surrounding the Gulf of Saros (Sarı and Çagatay, 2001). Candarli Gulf (Sta. 6, 7) on the Eastern Aegean coast has a medial coordinate at 38° 560 N latitude and 26° 570 E longitude. The Gulf has been strongly affected by growing population and industrialization. Major industrial developments located in the coastal area of Candarli, have been discharging solid and liquid wastes into Bakircay or Candarli Gulf or after minimal treatment. The intense maritime traffic together with untreated domestic discharges from
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F. Kucuksezgin et al. / Marine Pollution Bulletin 62 (2011) 1984–1988
Table 2 Butyltin compounds in biological tissues (ng Sn g1 wet weight) along the eastern Aegean coast. Species (n)
Site
Station no.
Length (mm)
MBT
DBT
TBT
BTs
Mytilus galloprovincialis(40) Mytilus galloprovincialis (38) Amphibalanus amphitrite (353) Amphibalanus amphitrite (170) Amphibalanus amphitrite (206) Mytilus galloprovincialis (40) Solea vulgaris (6) Mullus barbatus (12) Diplodus annularis (12) Solea vulgaris (6) Mullus barbatus (15) Mullus barbatus (6) Diplodus annularis (18) Mullus barbatus (20) Mullus barbatus (10) Diplodus annularis (20) Merluccius merluccius (10) Pagellus erythrinus (10) Amphibalanus amphitrite (299) Amphibalanus amphitrite (131) Mullus barbatus (16) Merluccius merluccius (12) Pagellus erythrinus (10)
Izmir Gulf-Pasaport Izmir Gulf-Pasaport
1 1 1 2 2 3 3 4 4 4 5 5 5 6 6 6 6 6 7 7 8 8 8
47.2 48.7 6 8 8 44.9 184 158 168 231 118 160 146 135 183 142 187 160 6 7 131 153 172
791 483 4819 3118 6346 895 1259 2876 2126 2230 1207 3344 2346 1323 1496 1760 2015 1687 4227 5353 1252 1862 2371
31.5 17.5 181.4 149.8 267 30.6 1.7 81.8 83.9 3.1 52.1 107.3 69.5 66.8 69.2 2.7 70.3 74.5 255.8 260.4 3.7 41.2 4.1
177 59 583 396 1163 111 181 318 275 260 134 368 252 259 174 186 198 276 512 564 156 157 327
1000 560 5583 3664 7776 1037 1442 3276 2485 2493 1393 3819 2668 1649 1739 1949 2283 2038 4995 6177 1412 2060 2702
Izmir Gulf-Levent Marina Izmir Gulf-Yenikale Izmir Gulf-Hekim adasi
Izmir Gulf-Uzunada
CandarliGulf
Saros Gulf
Table 3 Butyltin compounds in biological tissues (ng Sn g1) in Mediterranean harbors and marinas. Organism
Location
MBT
DBT
TBT
References
M. galloprovincialisa Deep sea fisha Oysterb H. trunculusb H. trunculusb M. barbatusb M. galloprovincialisa Fishb Mussela Mussela M. galloprovincialisa M. galloprovincialisa M. galloprovincialisa M. galloprovincialisa M. galloprovincialisa Mussel and claimb Balanus sp. Fishb M. galloprovincialisb Amphibalanus amphitriteb
Spain, Mediterranean Sea, 1996 Northwestern Mediterranean, Spain, 1996 South west coast, Spain, 1993–1994 South west coast, Spain, 1999 North-Western Sicilian coasts, Italy, 1999–2000 Aegean Sea, Greece, 2001–2003 Aegean Sea, Greece, 2001–2003 River Elbe and North Sea, 1993 Coast, Portugal, 1999–2000 Coast, Canada, 1995 Venice lagoon, Italy, 1999–2000 Venice lagoon, Italy, 1999–2003 Italy, Harbor, 2005 Slovenia, 2000–2006 Portuguese Coast, 2006 Portuguese Coast, 2006 Taiwan mariculture area Eastern Aegean coast, Turkey, 2009 Eastern Aegean coast, Turkey, 2009 Eastern Aegean coast, Turkey, 2009
10–204 nd–54 28.1 63 nd–167 <6–74 1.1–33 13–60 <7.9–41
4–1094 4–67 59.3 85 nd–316 21–366 5.5–31 12–28 <2.5–18
1–1151 1–52 269 48 nd–91 <4–109 <4–58 27–202 5.7–489 20–1198 nd–4500 16–2732 570 36–6434 93–420 1–720 238 134–368 59–177 396–1163
Morcillo and Porte (1998) Borghi and Porte (2002) Gomez-Ariza et al. (1997) Gomez-Ariza et al. (2006) Chiavarini et al. (2003) Chandrinou et al. (2006) Chandrinou et al. (2006) Shawky and Emons (1998) Diez et al. (2005) Chau et al. (1997) Bortoli et al. (2003) Zanon et al. (2009) Magi et al. (2008) Nemanicˇ et al. (2009) Sousa et al. (2009) Abd-Allah(1995) Liu et al., 2011 This study This study This study
nd: not detected. a Data expressed in dry weight basis. b Data expressed in wet weight basis.
the 200,000 inhabitants of the bay area further adds to sea contamination. Izmir Gulf (Western Turkey) is one of the great natural inlets of the Mediterranean. The Izmir Metropolitan Conurbation is an important industrial, commercial and cultural node. There is a large range of industrial activity including food processing, tanneries, paint, chemical, textile intersect manufacture and petroleum refining. The Gulf of Izmir has a total surface area of over 500 km2, a water capacity of 11.5 billion m3, and a total length of 64 km. The Levent Marina, Station 2 in the present research is positioned around the intersection of latitude 39° 42’N and longitude 27° 04’E on the south shore of the inner part of Izmir Gulf. The maximum depth in the Marina is only 5 m. Boat building and repair activities include all kinds of painting and maintenance such as varnishing, epoxy-polyester constructions, boat covering, spray-hood manufacture and repair. The servicing of all kinds of machinery and generators takes place.
Homogenized biota samples were prepared from pooled specimens recovered from the stations mapped in Fig. 1. Then, all samples were lyophilized before analysis. Using approximately 0.5 g aliquots of freeze-dried tissue, samples were made soluble in 10 ml tetra methyl ammonium hydroxide under agitation in an ultrasonic bath at 50 °C for 1.5 h (Cassi et al., 2002). Upon complete dissolution of tissues, a buffer and acetic acid were added to stabilize the pH at approximately 5–6. The samples were simultaneously derivatized and extracted using 1000 ll of sodium tetraethylborate (NaBEt4) and 5 ml of n-hexane. The samples were shaken for 10 min before being centrifuged at 5000 rpm for 15 min at 0 °C. The organic phase was recovered and a second extraction with 5 ml of n-hexane was performed followed by a further centrifugation. The organic phase was recovered and combined with the first one, and the extracts were then dried with pre-cleaned sodium sulfate and concentrated under a gentle stream of pure nitrogen. A clean-up of all samples was completed using solid
F. Kucuksezgin et al. / Marine Pollution Bulletin 62 (2011) 1984–1988
phase extraction cartridges filled with 1 g of florisil and eluted with 10 ml of n-hexane. The purified samples were then concentrated with a gentle stream of pure nitrogen prior to analysis by gas chromatography. The organotin compounds were determined by gas chromatography using a mass spectrometer detector (Agilent 6850GC-5973MSD). Separations were carried out by means of an HP-5MS column (30 m 0.25 mm i.d. 0.25 lm film thickness) under a helium flow rate of 1.2 ml min1. The temperature program was 60 °C for 2 min, 60–270 °C for 6 min, 270 °C for 20 min. Under such conditions, the following organotin species were resolved: MBT, DBT and TBT. A quality control system based on three internal standards was adopted (Cassi et al., 2002). Tripropyltin was used to indicate the derivatisation reaction efficiency. Tetraoctyltin was used to check the overall solvent extraction efficiency. Both internal standards were spiked just prior to leaching. Tetrabutyltin, spiked in all samples prior to injection, was used as a GC-internal standard to quantify the recoveries of both internal standards. Appropriate blanks were analyzed with each batch of samples and, in addition, reference materials were determined simultaneously. ERM-CE477 (mussel tissue) was used for biota samples and certified; observed values are given in Table 1. The detection limits for organotin species in biota limits (ng Sn g1 dry weight) were MBT 0.57–5.5, DBT 0.56–5.1, TBT 0.8–4.0. Concentrations of BT compounds determined in fish, mussels and barnacles at sampling sites are shown in Table 2. The TBT in the body burden content of M. barbatus varied between 134 and 368 ng Sn g1 wet weight (ww), MBT ranged from 1207 to 3344 ng g1 whereas DBT ranged from 3.7 to 107.3 ng Sn g1 ww. TBT concentrations ranged between 186–275, 157–198, 181–260, 276–327 ng Sn g1 ww for D. annularis, M. merluccius, S. vulgaris, P. erythrinus, respectively. The lowest TBT and MBT concentrations were found in mussels (TBT: 59–177 ng g1 ww). Total BTs concentrations, and in particular the TBT, in barnacles were generally higher (396–1163 ng g1 ww) than those monitored in the mussel and fish species sampled along the Eastern Aegean coast. Indeed, experimental evidence indicates that TBT can be directly ingested from contaminated sediments by scavenger organisms such as gastropods and mussels (Langston, 1996; Berto et al., 2007). BT concentrations in M. barbatus, which feeds on small benthic invertebrates and in barnacles are moderately high along the Eastern Aegean coast. MBT was the dominant species in mussels, fish and barnacles (Table 2), suggesting a relatively higher rate of metabolism of TBT. The partitioning pattern for MBT was dominant in the biota. This may indicate that MBT is derived not only from the dominant breakdown product of TBT degradation but also from other sources, such as city sewage, industrial wastewater, etc. In Table 3, the levels of BTs found in biota samples in this study were compared with those recorded in other countries. The maximum concentrations of the three butyltins (TBT, DBT, MBT) species were monitored in mussels in Slovenia (TBT: 6434 ng Sn g1) and in the Venice Lagoon, Italy (TBT: 4500 ng Sn g1). Additionally, the lowest concentrations were found in deep sea fish and in Hexaplex trunculus in Spain. The values were lower in the Gulf of Izmir than those found in mussels from the Mediterranean proper. The values in the sampled fish species were found to have a range comparable with values monitored and reported in fish from the River Elbe and in the North Sea during the 1993 period (Diez et al., 2005). Seafood consumption varies greatly from country to country and from region to region (Belfroid et al., 2000). Thus, in order to improve our precise local understanding of the risk involved in the consumption of organotin-contaminated seafood, it is essential to take into consideration overall seafood consumption habits. It has been suggested that the best way to achieve this, is to use the calculation of the TARL. Average seafood consumption for
1987
Turkey has been given as 8 kg year1 (TUIK, 2009). Based on this average seafood consumption for Turkey, TARL was found to be 680 ng TBT g1 (279 ng Sn g1). A comparison of the results of the present study with the TARL indicated that three samples for fishes were found to exceed the TARL when only TBT is considered. However it exceeded in seven samples if the sum of TBT + DBT is used. Only S. vulgaris samples were below the TARL if both the sum of TBT + DBT and TBT were considered. For mussel samples, whole values were below the TARL, thus confirming that this group is the one posing no risk for consumers. But, in contrast all barnacle samples exceeded the approved TARL. TBT pollution has been observed in samples from many developing countries. Since there is great concern about the toxic effects of organotin in biota, more data about the accumulation and ecotoxicological implications of organotins along the food chain is needed. Tolerable average residue levels of TBT + DBT based on the average weight of 60 kg exceeded in 50% of the fish sampled. The levels of organotin compounds derived seafood in the Eastern Aegean coast of Turkey constitute ‘‘a risk to humans’’ as presently defined. Since the BT contents in mussel tissues did not exceed the TARL value, current ecotoxicological risks should be disregarded. Although bivalves are the most commonly used organisms as biomonitors, this study showed that barnacle A. amphitrite may be considered among the most sensitive organisms for biomonitoring programs due to their high accumulation capacity for absorbing BT compounds from their surroundings. References Abd-Allah, A.M., 1995. Occurrence of organotin compounds in water and biota from Alexandria harbors. Chemosphere 30, 707–715. Alzieu, C., Sanjuan, J., Deltreil, J.P., Borel, B., 1986. Tin contamination in Arcachon Bay: effects on oyster shell anomalies. Mar. Pollut. Bull. 17, 494–498. Beaumont, A.R., Newman, P.B., 1986. Low levels of tributyltin reduce growth of marine micro-algae. Mar. Pollut. Bull. 17, 457–461. Belfroid, A.C., Purperhart, M., Ariese, F., 2000. Organotin levels in seafood. Mar. Pollut. Bull. 40, 226–232. Berto, D., Giani, M., Boscolo, R., Covelli, S., Giovanardi, O., Massironi, M., Grassia, L., 2007. Organotins (TBT and DBT) in water, sediments, and gastropods of the southern Venice lagoon (Italy). Mar. Pollut. Bull. 55, 425–435. Borghi, V., Porte, C., 2002. Organotin pollution in deep-sea fish from the Northwestern Mediterranean. Environ. Sci. Technol. 36, 4224–4228. Bortoli, A., Troncon, A., Dariol, S., Pellizzato, F., Pavoni, B., 2003. Butyltins and phenyltins in biota and sediments from the Lagoon of Venice. Oceanologia 45, 7–23. Bowen, H.J.M., 1988. Tin. In: McKenzie, H.A., Smythe, L.E. (Eds.), Quantitative Trace Analysis of Biological Materials. Elsevier, Amsterdam, pp. 607–622. Cassi, R., Tolosa, I., Bartocci, J., de Mora, S.J., 2002. Organotin speciation analyses in marine biota using sodium tetraethylborate ethylation and gas chromatography with flame photometric detection. Appl. Organomet. Chem. 16, 355–359. Chandrinou, S., Stasinakis, A.S., Thomaidis, N.S., Nikolaou, A., Wegener, J.W., 2006. Distribution of organotin compounds in the bivalves of the Aegean Sea, Greece. Environ. Int. 33, 226–232. Chau, Y.K., Maguire, R.J., Brown, M., Yang, F., Batchelor, S.P., Thompson, J.A.J., 1997. Occurrence of butyltin compounds in mussels in Canada. Appl. Organomet. Chem. 11, 903–912. Chiavarini, S., Massanisso, P., Nicolai, P., Nobili, C., Morabito, R., 2003. Butyltins concentration levels and imposex occurrence in snails from the Sicilian coasts (Italy). Chemosphere 50, 311–319. Diez, S., Albanos, M., Bayona, M.J., 2002. Organotin contamination in sediments from the Western Mediterranean enclosures following 10 years of TBT regulation. Water Res. 36, 905–918. Diez, S., Lacorte, S., Viana, P., Barcelo, D., Bayona, J., 2005. Survey of organotin compounds in rivers and coastal environments in Portugal 1999–2000. Environ. Pollut. 136, 525–536. EU (Official Journal 15/12/2001). Decision No. 2455/2001/EC of the European Parliament and of the Council of 20 November 2001 Establishing the List of Priority Substances in the Field of Water Policy and Amending Directive 2000/ 60/EC (Text with EEA Relevance), 331, 0001-5. Fent, K., 1996. Ecotoxicology of organotin compounds. Crit. Rev. Toxicol. 26, 1–117. Gomez-Ariza, J.L., Morales, E., Giraldez, I., Beltran, R., Escobar, J.A.P., 1997. Acid/ extraction treatment of bivalves for organotin speciation. Fresenius J. Anal. Chem. 357, 1007–1009. Gomez-Ariza, J.L., Santos, M.M., Morales, E., Giraldez, I., Sánchez-Rodas, D., Vieira, N., Kemp, J.F., Boon, J.P., Ten-Hallers-Tjabbes, C.C., 2006. Organotin contamination in the Atlantic Ocean of the Iberian Peninsula in relation to shipping. Chemosphere 64, 1100–1108.
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Assessment of organotin (butyltin species) contamination in marine biota from the Eastern Aegean Sea, Turkey F. Kucuksezgin ⇑, S. Aydin-Onen, L.T. Gonul, I. Pazi, F. Kocak Dokuz Eylul University, Institute of Marine Sciences and Technology, Inciralti, 35340 Izmir, Turkey
a r t i c l e Keywords: Butyltins Fish Mussel Barnacle TARL Eastern Aegean Sea
i n f o
a b s t r a c t The marine environment continues to be adversely affected by tributyltin (TBT) release from maritime traffic. Therefore the concentrations of TBT, dibutyltin (DBT) and monobutyltin (MBT) were measured in barnacles, mussels and fish along the Eastern Aegean coastline. The average concentrations of TBT ng Sn g1 were found to be 235 in fish, 116 in mussels and 635 in barnacles. The highest concentrations of TBT, DBT and MBT were observed in the barnacles which had been sampled in marinas and harbors. All mussels sampled showed values of TBT + DBT, which were below the ‘‘tolerable average residue level (TARL)’’ as currently accepted. This indicates a lack of risk to the consumer. However, 7 out of the 15 fish sampled displayed TBT + DBT levels above the TARL, which indicates that a fish consumer group may be at risk. Barnacles have high potential as biomonitors for the presence of organotin in the Aegean Sea. Ó 2011 Elsevier Ltd. All rights reserved.
Since the early 1960s organotin compounds (OTs) have been used for several purposes, such as polyvinyl chloride (PVC) stabilizers, wood preserving agents, fungicides in agricultural activities, catalysts in the production of polyurethane foams and as antifouling agents in ship paints (Fent, 1996; Wang et al., 2008). Moreover organotin compounds, due to their lipid solubility, may penetrate tissues and enter the central nervous system with great potentially toxicity to organisms (Bowen, 1988). Thus, the occurrence and the impact of organotin compounds in the environment (mostly the butyl species), in is of great concern. Due to their broad range of industrial and agrochemical applications, organotin compounds have entered a number of ecosystems in considerable amounts (Hoch, 2001). Various biological effects on non-target aquatic organisms as a result of exposure to OTs have been documented. These include reduction of growth (Salazar and Salazar, 1991); larval mortality (Tanabe et al., 2000; Zhou et al., 2003); shell thickening (Alzieu et al., 1986); low progesterone levels and delay in sexual maturation (Siah et al., 2003); imposex in gastropods, mussels, microalgae and snails (Beaumont and Newman, 1986; Zhou et al., 2003) and immunological dysfunction in fish (Zhou et al., 2003). This toxicity was related to exposure concentration and duration; to bioavailability, to the sensitivity of the organisms (Rudel, 2003) and to their bioaccumulative potential (Takahashi et al., 1999). Bivalves are the organisms most employed as biomonitors, accumulating OTs in direct proportion to environmental levels (Zhou et al., 2003; Harino et al., 2005). They are considered to be ⇑ Corresponding author. Tel.: +90 2322785565; fax: +90 2322785082. E-mail address: fi[email protected] (F. Kucuksezgin). 0025-326X/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2011.06.020
a reliable indicator of biochemical conditions in the marine environment because of their tendency to absorb and accumulate a wide range of chemicals from their surroundings (Tanabe et al., 2000). Chemicals enter bivalves through their intake of food and water and are released from them via excretion and depuration back to the water (O’Connor, 2002). Many countries worldwide have banned the application of TBTbased paints to small vessels (<25 m) and butyltins have been identified as priority hazardous substances (EU, 2001). Moreover, negotiations at the International Maritime Organization (IMO) resulted in a resolution calling for a global prohibition on the application of OT compounds in antifouling systems on ships by January 2003 and a complete prohibition by January 2008 (Rudel, 2003). Due to the ongoing legislative restrictions, various studies worldwide have shown a slow decline on TBT contamination (Hoch, 2001). Present and future restrictions will not immediately remove the TBT and its degradation products (dibutyltin and monobutyltin, DBT and MBT) from the marine environment; since these compounds are persistently retained in the sediments (Diez et al., 2002). The hot spots for TBT release in the Mediterranean are be associated with the major commercial harbors in the region (UNEP, 2002). Despite an extensive number of studies on the negative impact of TBT in marine organisms, few works exist in Europe reporting the levels of these compounds in edible fish (Shawky and Emons, 1998; Borghi and Porte, 2002; Chandrinou et al., 2006). There have been a few studies on the distribution of butyltin concentrations in Turkish coastal areas. TBT concentrations in seawater samples collected along the Turkish coast of the Mediterranean Sea have been highly variable over time and space
F. Kucuksezgin et al. / Marine Pollution Bulletin 62 (2011) 1984–1988
1985
Fig. 1. Location of sampling points.
Table 1 Results for reference material (ERM-CE477) as mg/kg dry weight. BTs
Certified value
Observed value
MBT DBT TBT
1.50 ± 0.28 1.54 ± 0.12 2.20 ± 0.19
1.57 ± 0.035 1.52 ± 0.064 1.92 ± 0.20
(bdl-33.18 ng Sn l1). The highest values have been measured in water sampled from harbors and marinas (Kubilay et al., 1996; Yemenicioglu and de Mora, 2009). This present study aims firstly to create a baseline regarding organotin levels and total tin concentrations in mussel, barnacle and fish tissues; secondly to gather more information on the use of selected species as biomonitors and finally to evaluate potential risks for BT species contamination in seafood along the Eastern Aegean coast as sampled in 2009. After reviewing the open literature on TBT toxicity Penninks (1993), derived that the TDI is 0.25 lg/kg bodyweight (bw)/day. This value is based on the observed effect of TBT on the immune function in rats. The value of 0.25 lg TBT/kg-bw/day derived by Penninks (1993) is generally accepted and referred by Kannan and Falandysz (1997), Robinson et al. (1999) and Belfroid et al. (2000). Based on the TDI of 0.25 lg/kg bw/day for TBT the maximum TDI TBT intake is 15 lg per day for a person with an average body weight of 60 kg (Kannan and Falandysz, 1997). The TARL is defined as the level in seafood that is tolerable for the average consumer with an average weight of 60 kg. This newly developed tool can be calculated according to:
TARL ¼ ðTDI 60 kg bwÞ=average daily seafood consumption
The advantage of this approach is that the TARL value can be compared directly with measured residue levels of TBT in seafood. In addition, TARL values can be the basis for appropriate authorities to derive and define the maximum residue limit (MRL) of TBT in seafood for the purposes of legislation (Belfroid et al., 2000). In the present study, different marine species (Mytilus galloprovincialis, Amphibalanus amphitrite, Mullus barbatus, Diplodus annularis, Merluccius merluccius, Solea vulgaris and Pagellus erythrinus) were sampled for BTs analysis in terms of their different feeding strategies. Samples were collected from the Saros, Candarli and Izmir Gulfs along the Eastern Aegean coast, during 2009 (Fig. 1). Izmir Gulf was represented by five sampling stations. Three of them were located in the inner part of the Gulf (Sta. 1, 2, 3), while two stations were selected (4, 5) in the outer part of the Gulf. The Gulf of Saros (Sta. 8) is located in the North Eastern Aegean Sea and has an asymmetric bathymetry with a 10 km wide shelf to the north and up to 15 km wide trough in the south. The shelf extends at a water depth of 90–120 m. Several major rivers discharge into the Saros Gulf such as Meriç River and Kavak Creek. However, there is no industry or significant settlement in the area surrounding the Gulf of Saros (Sarı and Çagatay, 2001). Candarli Gulf (Sta. 6, 7) on the Eastern Aegean coast has a medial coordinate at 38° 560 N latitude and 26° 570 E longitude. The Gulf has been strongly affected by growing population and industrialization. Major industrial developments located in the coastal area of Candarli, have been discharging solid and liquid wastes into Bakircay or Candarli Gulf or after minimal treatment. The intense maritime traffic together with untreated domestic discharges from
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Table 2 Butyltin compounds in biological tissues (ng Sn g1 wet weight) along the eastern Aegean coast. Species (n)
Site
Station no.
Length (mm)
MBT
DBT
TBT
BTs
Mytilus galloprovincialis(40) Mytilus galloprovincialis (38) Amphibalanus amphitrite (353) Amphibalanus amphitrite (170) Amphibalanus amphitrite (206) Mytilus galloprovincialis (40) Solea vulgaris (6) Mullus barbatus (12) Diplodus annularis (12) Solea vulgaris (6) Mullus barbatus (15) Mullus barbatus (6) Diplodus annularis (18) Mullus barbatus (20) Mullus barbatus (10) Diplodus annularis (20) Merluccius merluccius (10) Pagellus erythrinus (10) Amphibalanus amphitrite (299) Amphibalanus amphitrite (131) Mullus barbatus (16) Merluccius merluccius (12) Pagellus erythrinus (10)
Izmir Gulf-Pasaport Izmir Gulf-Pasaport
1 1 1 2 2 3 3 4 4 4 5 5 5 6 6 6 6 6 7 7 8 8 8
47.2 48.7 6 8 8 44.9 184 158 168 231 118 160 146 135 183 142 187 160 6 7 131 153 172
791 483 4819 3118 6346 895 1259 2876 2126 2230 1207 3344 2346 1323 1496 1760 2015 1687 4227 5353 1252 1862 2371
31.5 17.5 181.4 149.8 267 30.6 1.7 81.8 83.9 3.1 52.1 107.3 69.5 66.8 69.2 2.7 70.3 74.5 255.8 260.4 3.7 41.2 4.1
177 59 583 396 1163 111 181 318 275 260 134 368 252 259 174 186 198 276 512 564 156 157 327
1000 560 5583 3664 7776 1037 1442 3276 2485 2493 1393 3819 2668 1649 1739 1949 2283 2038 4995 6177 1412 2060 2702
Izmir Gulf-Levent Marina Izmir Gulf-Yenikale Izmir Gulf-Hekim adasi
Izmir Gulf-Uzunada
CandarliGulf
Saros Gulf
Table 3 Butyltin compounds in biological tissues (ng Sn g1) in Mediterranean harbors and marinas. Organism
Location
MBT
DBT
TBT
References
M. galloprovincialisa Deep sea fisha Oysterb H. trunculusb H. trunculusb M. barbatusb M. galloprovincialisa Fishb Mussela Mussela M. galloprovincialisa M. galloprovincialisa M. galloprovincialisa M. galloprovincialisa M. galloprovincialisa Mussel and claimb Balanus sp. Fishb M. galloprovincialisb Amphibalanus amphitriteb
Spain, Mediterranean Sea, 1996 Northwestern Mediterranean, Spain, 1996 South west coast, Spain, 1993–1994 South west coast, Spain, 1999 North-Western Sicilian coasts, Italy, 1999–2000 Aegean Sea, Greece, 2001–2003 Aegean Sea, Greece, 2001–2003 River Elbe and North Sea, 1993 Coast, Portugal, 1999–2000 Coast, Canada, 1995 Venice lagoon, Italy, 1999–2000 Venice lagoon, Italy, 1999–2003 Italy, Harbor, 2005 Slovenia, 2000–2006 Portuguese Coast, 2006 Portuguese Coast, 2006 Taiwan mariculture area Eastern Aegean coast, Turkey, 2009 Eastern Aegean coast, Turkey, 2009 Eastern Aegean coast, Turkey, 2009
10–204 nd–54 28.1 63 nd–167 <6–74 1.1–33 13–60 <7.9–41
4–1094 4–67 59.3 85 nd–316 21–366 5.5–31 12–28 <2.5–18
1–1151 1–52 269 48 nd–91 <4–109 <4–58 27–202 5.7–489 20–1198 nd–4500 16–2732 570 36–6434 93–420 1–720 238 134–368 59–177 396–1163
Morcillo and Porte (1998) Borghi and Porte (2002) Gomez-Ariza et al. (1997) Gomez-Ariza et al. (2006) Chiavarini et al. (2003) Chandrinou et al. (2006) Chandrinou et al. (2006) Shawky and Emons (1998) Diez et al. (2005) Chau et al. (1997) Bortoli et al. (2003) Zanon et al. (2009) Magi et al. (2008) Nemanicˇ et al. (2009) Sousa et al. (2009) Abd-Allah(1995) Liu et al., 2011 This study This study This study
nd: not detected. a Data expressed in dry weight basis. b Data expressed in wet weight basis.
the 200,000 inhabitants of the bay area further adds to sea contamination. Izmir Gulf (Western Turkey) is one of the great natural inlets of the Mediterranean. The Izmir Metropolitan Conurbation is an important industrial, commercial and cultural node. There is a large range of industrial activity including food processing, tanneries, paint, chemical, textile intersect manufacture and petroleum refining. The Gulf of Izmir has a total surface area of over 500 km2, a water capacity of 11.5 billion m3, and a total length of 64 km. The Levent Marina, Station 2 in the present research is positioned around the intersection of latitude 39° 42’N and longitude 27° 04’E on the south shore of the inner part of Izmir Gulf. The maximum depth in the Marina is only 5 m. Boat building and repair activities include all kinds of painting and maintenance such as varnishing, epoxy-polyester constructions, boat covering, spray-hood manufacture and repair. The servicing of all kinds of machinery and generators takes place.
Homogenized biota samples were prepared from pooled specimens recovered from the stations mapped in Fig. 1. Then, all samples were lyophilized before analysis. Using approximately 0.5 g aliquots of freeze-dried tissue, samples were made soluble in 10 ml tetra methyl ammonium hydroxide under agitation in an ultrasonic bath at 50 °C for 1.5 h (Cassi et al., 2002). Upon complete dissolution of tissues, a buffer and acetic acid were added to stabilize the pH at approximately 5–6. The samples were simultaneously derivatized and extracted using 1000 ll of sodium tetraethylborate (NaBEt4) and 5 ml of n-hexane. The samples were shaken for 10 min before being centrifuged at 5000 rpm for 15 min at 0 °C. The organic phase was recovered and a second extraction with 5 ml of n-hexane was performed followed by a further centrifugation. The organic phase was recovered and combined with the first one, and the extracts were then dried with pre-cleaned sodium sulfate and concentrated under a gentle stream of pure nitrogen. A clean-up of all samples was completed using solid
F. Kucuksezgin et al. / Marine Pollution Bulletin 62 (2011) 1984–1988
phase extraction cartridges filled with 1 g of florisil and eluted with 10 ml of n-hexane. The purified samples were then concentrated with a gentle stream of pure nitrogen prior to analysis by gas chromatography. The organotin compounds were determined by gas chromatography using a mass spectrometer detector (Agilent 6850GC-5973MSD). Separations were carried out by means of an HP-5MS column (30 m 0.25 mm i.d. 0.25 lm film thickness) under a helium flow rate of 1.2 ml min1. The temperature program was 60 °C for 2 min, 60–270 °C for 6 min, 270 °C for 20 min. Under such conditions, the following organotin species were resolved: MBT, DBT and TBT. A quality control system based on three internal standards was adopted (Cassi et al., 2002). Tripropyltin was used to indicate the derivatisation reaction efficiency. Tetraoctyltin was used to check the overall solvent extraction efficiency. Both internal standards were spiked just prior to leaching. Tetrabutyltin, spiked in all samples prior to injection, was used as a GC-internal standard to quantify the recoveries of both internal standards. Appropriate blanks were analyzed with each batch of samples and, in addition, reference materials were determined simultaneously. ERM-CE477 (mussel tissue) was used for biota samples and certified; observed values are given in Table 1. The detection limits for organotin species in biota limits (ng Sn g1 dry weight) were MBT 0.57–5.5, DBT 0.56–5.1, TBT 0.8–4.0. Concentrations of BT compounds determined in fish, mussels and barnacles at sampling sites are shown in Table 2. The TBT in the body burden content of M. barbatus varied between 134 and 368 ng Sn g1 wet weight (ww), MBT ranged from 1207 to 3344 ng g1 whereas DBT ranged from 3.7 to 107.3 ng Sn g1 ww. TBT concentrations ranged between 186–275, 157–198, 181–260, 276–327 ng Sn g1 ww for D. annularis, M. merluccius, S. vulgaris, P. erythrinus, respectively. The lowest TBT and MBT concentrations were found in mussels (TBT: 59–177 ng g1 ww). Total BTs concentrations, and in particular the TBT, in barnacles were generally higher (396–1163 ng g1 ww) than those monitored in the mussel and fish species sampled along the Eastern Aegean coast. Indeed, experimental evidence indicates that TBT can be directly ingested from contaminated sediments by scavenger organisms such as gastropods and mussels (Langston, 1996; Berto et al., 2007). BT concentrations in M. barbatus, which feeds on small benthic invertebrates and in barnacles are moderately high along the Eastern Aegean coast. MBT was the dominant species in mussels, fish and barnacles (Table 2), suggesting a relatively higher rate of metabolism of TBT. The partitioning pattern for MBT was dominant in the biota. This may indicate that MBT is derived not only from the dominant breakdown product of TBT degradation but also from other sources, such as city sewage, industrial wastewater, etc. In Table 3, the levels of BTs found in biota samples in this study were compared with those recorded in other countries. The maximum concentrations of the three butyltins (TBT, DBT, MBT) species were monitored in mussels in Slovenia (TBT: 6434 ng Sn g1) and in the Venice Lagoon, Italy (TBT: 4500 ng Sn g1). Additionally, the lowest concentrations were found in deep sea fish and in Hexaplex trunculus in Spain. The values were lower in the Gulf of Izmir than those found in mussels from the Mediterranean proper. The values in the sampled fish species were found to have a range comparable with values monitored and reported in fish from the River Elbe and in the North Sea during the 1993 period (Diez et al., 2005). Seafood consumption varies greatly from country to country and from region to region (Belfroid et al., 2000). Thus, in order to improve our precise local understanding of the risk involved in the consumption of organotin-contaminated seafood, it is essential to take into consideration overall seafood consumption habits. It has been suggested that the best way to achieve this, is to use the calculation of the TARL. Average seafood consumption for
1987
Turkey has been given as 8 kg year1 (TUIK, 2009). Based on this average seafood consumption for Turkey, TARL was found to be 680 ng TBT g1 (279 ng Sn g1). A comparison of the results of the present study with the TARL indicated that three samples for fishes were found to exceed the TARL when only TBT is considered. However it exceeded in seven samples if the sum of TBT + DBT is used. Only S. vulgaris samples were below the TARL if both the sum of TBT + DBT and TBT were considered. For mussel samples, whole values were below the TARL, thus confirming that this group is the one posing no risk for consumers. But, in contrast all barnacle samples exceeded the approved TARL. TBT pollution has been observed in samples from many developing countries. Since there is great concern about the toxic effects of organotin in biota, more data about the accumulation and ecotoxicological implications of organotins along the food chain is needed. Tolerable average residue levels of TBT + DBT based on the average weight of 60 kg exceeded in 50% of the fish sampled. The levels of organotin compounds derived seafood in the Eastern Aegean coast of Turkey constitute ‘‘a risk to humans’’ as presently defined. Since the BT contents in mussel tissues did not exceed the TARL value, current ecotoxicological risks should be disregarded. Although bivalves are the most commonly used organisms as biomonitors, this study showed that barnacle A. amphitrite may be considered among the most sensitive organisms for biomonitoring programs due to their high accumulation capacity for absorbing BT compounds from their surroundings. References Abd-Allah, A.M., 1995. Occurrence of organotin compounds in water and biota from Alexandria harbors. Chemosphere 30, 707–715. Alzieu, C., Sanjuan, J., Deltreil, J.P., Borel, B., 1986. Tin contamination in Arcachon Bay: effects on oyster shell anomalies. Mar. Pollut. Bull. 17, 494–498. Beaumont, A.R., Newman, P.B., 1986. Low levels of tributyltin reduce growth of marine micro-algae. Mar. Pollut. Bull. 17, 457–461. Belfroid, A.C., Purperhart, M., Ariese, F., 2000. Organotin levels in seafood. Mar. Pollut. Bull. 40, 226–232. Berto, D., Giani, M., Boscolo, R., Covelli, S., Giovanardi, O., Massironi, M., Grassia, L., 2007. Organotins (TBT and DBT) in water, sediments, and gastropods of the southern Venice lagoon (Italy). Mar. Pollut. Bull. 55, 425–435. Borghi, V., Porte, C., 2002. Organotin pollution in deep-sea fish from the Northwestern Mediterranean. Environ. Sci. Technol. 36, 4224–4228. Bortoli, A., Troncon, A., Dariol, S., Pellizzato, F., Pavoni, B., 2003. Butyltins and phenyltins in biota and sediments from the Lagoon of Venice. Oceanologia 45, 7–23. Bowen, H.J.M., 1988. Tin. In: McKenzie, H.A., Smythe, L.E. (Eds.), Quantitative Trace Analysis of Biological Materials. Elsevier, Amsterdam, pp. 607–622. Cassi, R., Tolosa, I., Bartocci, J., de Mora, S.J., 2002. Organotin speciation analyses in marine biota using sodium tetraethylborate ethylation and gas chromatography with flame photometric detection. Appl. Organomet. Chem. 16, 355–359. Chandrinou, S., Stasinakis, A.S., Thomaidis, N.S., Nikolaou, A., Wegener, J.W., 2006. Distribution of organotin compounds in the bivalves of the Aegean Sea, Greece. Environ. Int. 33, 226–232. Chau, Y.K., Maguire, R.J., Brown, M., Yang, F., Batchelor, S.P., Thompson, J.A.J., 1997. Occurrence of butyltin compounds in mussels in Canada. Appl. Organomet. Chem. 11, 903–912. Chiavarini, S., Massanisso, P., Nicolai, P., Nobili, C., Morabito, R., 2003. Butyltins concentration levels and imposex occurrence in snails from the Sicilian coasts (Italy). Chemosphere 50, 311–319. Diez, S., Albanos, M., Bayona, M.J., 2002. Organotin contamination in sediments from the Western Mediterranean enclosures following 10 years of TBT regulation. Water Res. 36, 905–918. Diez, S., Lacorte, S., Viana, P., Barcelo, D., Bayona, J., 2005. Survey of organotin compounds in rivers and coastal environments in Portugal 1999–2000. Environ. Pollut. 136, 525–536. EU (Official Journal 15/12/2001). Decision No. 2455/2001/EC of the European Parliament and of the Council of 20 November 2001 Establishing the List of Priority Substances in the Field of Water Policy and Amending Directive 2000/ 60/EC (Text with EEA Relevance), 331, 0001-5. Fent, K., 1996. Ecotoxicology of organotin compounds. Crit. Rev. Toxicol. 26, 1–117. Gomez-Ariza, J.L., Morales, E., Giraldez, I., Beltran, R., Escobar, J.A.P., 1997. Acid/ extraction treatment of bivalves for organotin speciation. Fresenius J. Anal. Chem. 357, 1007–1009. Gomez-Ariza, J.L., Santos, M.M., Morales, E., Giraldez, I., Sánchez-Rodas, D., Vieira, N., Kemp, J.F., Boon, J.P., Ten-Hallers-Tjabbes, C.C., 2006. Organotin contamination in the Atlantic Ocean of the Iberian Peninsula in relation to shipping. Chemosphere 64, 1100–1108.
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