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Distribution and accumulation of organotin species in seawater, sedimentsand organisms collected from a Taiwan mariculture area

Li-Lian Liu a, Jih-Terng Wang b, Kuo-Nan Chung c, Ming-Yih Leu d,e,⇑, Pei-Jie Meng d,e,⇑a Institute of Marine Biology and Asia-Pacific Ocean Research Center, Kuroshio Research Group, National Sun Yat-Sen University, Kaohsiung 80424, Taiwanb Department of Biotechnology, Tajen University, Pingtung 907, Taiwanc Institute of Public Affairs Management, National Sun Yat-Sen University, Kaohsiung 80424, Taiwand National Museum of Marine Biology and Aquarium, Checheng 944, Taiwane Graduate Institute of Marine Biodiversity and Evolutionary Biology, National Dong Hwa University, Checheng 944, Taiwan

a r t i c l e i n f o

Keywords:BioaccumulationCage maricultureOrganotin compoundsTributyltin

a b s t r a c t

The present study was undertaken to evaluate the distribution and accumulation of tributyltin (TBT) andtriphenyltin (TPhT) in seawater, sediments and selected organisms from a cage mariculture area in south-ern Taiwan, Hsiao Liouchiou Island. Our results show that ROTs were found in concentrations as high as196 ng/L in seawater collected from the sites in Pai-Sa harbor, and up 1040 ng/g dry wt. in sedimentsdredged from sites within Da-Fu harbor. Also, ROTs concentrations of 859 ng/g dry wt. were observedin the liver of cobia (Rachycentron canadum) from mariculture cages. As most published studies havefocused on the acute toxicity and bioaccumulation of organotins in mussels, the effects of organotinson cobia and other marine fauna are still poorly understood. This study highlights the significance ofRBTs accumulation in cobia, as well as in the sediments and seawater surrounding their culture facilities.

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1. Introduction

Since tributyltin (TBT) was first used as a pesticide in 1925(Thompson et al., 1985), an increasing number of organotin com-pounds have been produced and used as biocides (e.g., antifoulingpaints for ships) and stabilizers for polyvinyl chloride polymers(Evans and Karpel, 1985). Consequently, these organotin com-pounds have become increasingly serious pollutants in coastalareas (Meinema et al., 1986; Alzieu, 1989, 1991, 2000; Salazerand Salazer, 1991; Iwata et al., 1995). TBT and triphenyltin (TPhT)can be degraded to dibutyltin (DBT), monobutyltin (MBT),diphenyltin (DPhT) and monophenyltin (MPhT) by solar radiation,bacterial biodegradation, and/or biological decomposition(Maguire et al., 1983), and the latter species are also consideredto be pollutants.

While it is difficult to estimate the consumption and conse-quent release of TBT and TPhT, the Taiwan Agriculture IndustryAssociation (TAIA, 1997) indicated that more than 150 tons of45% and 20 tons of 2% TPhT acetate were used for agricultural pro-tection in 1996. However, ship building and repairing industries, as

well as transiting vessels, contribute unknown quantities oforganotins into the Taiwan Strait. Therefore, it is not surprisingthat high concentrations of TBT (as high as 2500 ng/g dry wt.) werefound in sediments from Keelung harbor (Hung and Liu, 1998).Likewise, high TBT concentrations (up to 1660 ng/g) were observedin oysters (Crassostrea gigas) from the Shiangsan mariculture areain northern Taiwan (Hung et al., 1998). Extremely high levels ofTBT were obtained in hermaphroditic oyster samples collected insummer and autumn 1999, as well as in winter 2000 (Hung etal., 2000).

Organotins, especially TBT, are highly toxic towards marineorganisms. For instance, a number of studies have shown that evenppb levels of TBTs caused oyster shell anomalies and spat settle-ment failure (Alzieu, 1986, 1991, 2000). Additional detrimental im-pacts of TBT have been documented (Hung et al., 1998, 2000, 2001;Wilken et al., 1994; Fent and Meier, 1994; Horiguchi et al., 1994;Bryan et al., 1986; Meng et al., 2003, 2005). However, few studieshave been conducted on the distribution and accumulation of TBTand TPhT in cobia (Rachycentron canadum) from cage maricultureareas (Liu et al., 2006). Not only is cobia a delicacy, it also growsvery quickly. These characteristics make cobia an appealing aqua-culture species. Commercial production of cobia already has a suc-cessful history in Asia, most notably in Taiwan where it is stockedin around 80% of ocean cages. Given the possible detrimental im-pacts of TBT and related compounds on cobia, and potentially othermarine fauna, the purpose of this study was to evaluate the distri-bution and accumulation of TBT and TPhT in seawater, sediments

0025-326X/$ - see front matter � 2011 Elsevier Ltd. All rights reserved.doi:10.1016/j.marpolbul.2011.02.003

⇑ Corresponding authors. Address: Graduate Institute of Marine Biodiversity andEvolutionary Biology, National Dong Hwa University, Checheng 944, Taiwan.Tel.: +886 8 8825034; fax: 886 8 8825066 (P.-J. Meng), tel.: +886 8 8825385; fax:886 8 8825066 (M.-Y. Leu).

E-mail addresses: myl@nmmba.gov.tw (M.-Y. Leu), pjmeng@nmmba.gov.tw(P.-J. Meng).

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and organisms from a cage mariculture environment of southernTaiwan, Hsiao Liouchiou Island.

2. Experimental methods

Triplicate samples of seawater, sediments and organisms werecollected at 10 sites along the coast of Hsiao Liouchiou Island,southern Taiwan (Fig. 1). Immediately after collection, the sampleswere transferred to the Marine Chemistry Laboratory of Taiwan’sNational Museum of Marine Biology and Aquarium (NMMBA) foranalysis.

Specimens of R. canadum with body lengths of 80 ± 5 cm andtwo species of sessile barnacles, Balanus sp. and Lepas anserifera,were collected at Station S4 (Fig. 1), which is within a cage aqua-culture area. Immediately after collection, fish samples were frozenat �20 �C and dissected to separate red muscle, abdominal muscle,dorsal muscle, stomach, gill, liver, kidney and gonads. Fish sectionsand whole barnacle tissues were washed with seawater, blotteddry with cheese-cloth, and then processed for organotin speciesanalysis (described below). Surface water samples were taken withmetal-free Niskin bottles and kept at 4 �C until analysis. Surfacesediment samples were collected by dredging and stored in plasticbags at 4 �C until analysis.

Animal tissues and sediments were extracted in tropolone-ben-zene solution and levels of the following organotins were quanti-fied by the GC/FPD method (Hung and Liu, 1998; Hung et al.,1998; Meng et al., 2005): TBT, DBT, MBT, TPhT, DPhT and MPhT.Organotin standards with purities ranging from 95% to 98% wereobtained from Aldrich–Chemie (Steinhein, Germany). Tetrabutyltinwas used as an internal standard for QA/QC of fish samples. Therecovery rates of TBT, DBT, MBT, TPhT, DPhT and MPhT were92.4 ± 6.9%, 93.5 ± 8.0%, 85.6 ± 4.0%, 70.4 ± 5.0%, 97.3 ± 10.8% and75.2 ± 7.0% (n = 3), respectively. Detection limits for TBT, DBT,MBT, TPhT, DPhT and MPhT were 9.1, 13.4, 8.1, 15.7, 7.2 and8.7 ng/g dry wt., respectively. The accuracy of the analytical meth-ods for determining TBT levels was verified using certified refer-ence biological material NIES-11 (Leteolabrax japonicus, Cuviertissue; 1.3 ± 0.1 lg/g). The measured value and recovery rate forTBT were 1.28 ± 0.05 lg/g and 98.5% (n = 3), respectively (Meng

et al., 2005). For the barnacles, European reference material(ERM) CE477 (mussel tissue) was used for QA/QC. The averagerecoveries (n = 3) for TBT, DBT and MBT were 88.2 ± 3.6%,99.4 ± 3.9%, and 115 ± 4.0%, respectively. The detection limits ofthis method on a dry weight basis were 8.7 ng/g for TBT, 7.8 ng/gfor DBT, 1.8 ng/g for MBT, 4.0 ng/g for TPhT, 3.3 ng/g for DPhTand 2.0 ng/g for MPhT. The accuracy and precision were 88.2%and 3.6%, respectively, for TBT. For the sediment, the coastal sedi-ment (CRM 462) was to be used as a certified reference material.The average recoveries (n = 3) for TBT and DBT were 92.2 ± 4.7%and 94.3 ± 3.8%. The detection limits of sediments on a dry weightbasis were 3.2 ng/g for TBT, 1.5 ng/g for DBT, 5.0 ng/g for MBT,4.7 ng/g for TPhT, 0.5 ng/g for DPhT and 0.5 ng/g for MPhT. Thedetection limits of seawater were 5.7 ng/L for TBT, 2.1 ng/L forDBT, 3.1 ng/L for MBT, 7.0 ng/L for TPhT, 4.0 ng/L for DPhT and1.0 ng/L for MPhT. The general bioconcentration factor (BCF) model(Holdway et al., 1983) was used to examine the accumulation oforganotins in R. canadum, Balanus sp. and L. anserifera.

3. Results and discussion

Samples of seawater and sediments were collected at 10 sitesaround the cage mariculture areas along the coast of Hsiao Liou-ciou Island, southern Taiwan, and different organisms, R. canadum,Balanus sp. and L. anserifera, were collected directly from maricul-ture cages. Organotin species were analyzed by the GC/FPD meth-od. The ROTs (sum of TBT, DBT, MBT, TPhT, DPhT and MPhT) inseawater ranged between 43.8 and 196 ng/L (Table 1). The concen-trations of RBTs (sum of TBT, DBT and MBT) were notably higherthan RPhTs (sum of TPT, DPT, and MPT) in seawater. The concen-trations of ROTs in sediments ranged between 20.4 and 1038 ng/g (Table 2). PhTs were not detected in any sediment samples.

Extremely high concentrations of organotins were measured inboth seawater (160 and 196 ng/L) and sediments (895 and1038 ng/g) collected near Pai-Sa and Da-Fu harbors (sites 8 and9), respectively. On the contrary, lower concentrations of organo-tins both in seawater (ranging from 43.8 to 104 ng/L) and sedi-ments (20.4–49.8 ng/g) were observed at the other sampling sites(sites 0–7). Ship building and repairing industries, as well as trans-

Fig. 1. Locations of sampling sites along the coast of Hsiao Liouciou Island.

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iting vessels around Pai-Sa and Da-Fu harbor all contribute largequantities of organotins into the proximate marine environment.Phenyltins are common constituents of agricultural waste whilebutyltins (RBTs) are typically found at higher levels in coastal re-gions, especially near harbors (Hung et al., 1998; TAIA, 1997). Agri-culture is uncommon on Hsiao Liouciou Island. By contrast, thereare five ports and numerous mariculture pens. Therefore, it is notsurprising that butyltins were the dominant organotin speciesfound around the island.

Based on the percentage of 6 organotin species at the 10 sam-pling sites (Figs. 2 and 3), higher percentages of TBT both in seawa-ter (57.0% and 44.6%) and sediments (63.4% and 73.7%) wereobserved near Pai-Sa and Da-Fu harbors, respectively. The othersampling sites near the cage mariculture areas were characterized

by lower average percentages of TBT (26.4% and 18.0% in seawaterand sediments, respectively). In general, organisms located closerto the sources of pollution and/or with a shorter degradation timewill have higher percentage of TBT (Maguire et al., 1983). This sug-gests that the TBT and TPhT compounds can be gradually degradedto DBT, MBT, DPhT and MPhT and that their concentrations de-creased with distance from their deduced source, Pai-Sa and Da-Fu harbors.

The concentrations of RBTs in the barnacles Balanus sp. and L.anserifera collected at cage mariculture areas (Station S4 with 13cages) ranged between 357 and 336 ng/g (Table 3). These concen-trations were much lower than the concentrations of RBTs ob-served in oysters (C. gigas) from the Shiangsan mariculture area(as high as 1660 ng/g, Hung et al., 1998) and off the west coast

Table 1Concentrations (ng-Sn/g) of organotin species in seawater collected along the coast of Hsiao Liouciou Island.

Station No. MBT DBT TBT RBTs MPT DPT TPT RPhTs ROTs

0 12.9 ± 1.12 28.4 ± 2.53 21.6 ± 2.19 62.9 nd 26.1 ± 2.09 15.3 ± 1.43 41.4 1041 11.6 ± 0.97 18.5 ± 0.91 22.3 ± 2.21 52.4 nd 20.8 ± 1.49 nd 20.8 73.22 12.5 ± 1.64 14.0 ± 1.35 17.7 ± 0.88 44.2 nd 15.7 ± 1.01 nd 15.7 59.93 17.0 ± 1.16 12.3 ± 0.49 15.0 ± 0.50 44.3 nd 9.16 ± 0.52 nd 9.16 53.54 11.8 ± 1.13 15.7 ± 1.13 28.8 ± 3.67 56.3 nd 7.70 ± 0.39 12.7 ± 0.99 20.4 76.75 11.6 ± 0.95 26.6 ± 1.39 6.88 ± 0.52 45.1 nd 7.97 ± 0.68 nd 7.97 53.16 4.20 ± 0.20 15.5 ± 1.78 14.5 ± 1.30 34.2 nd 9.58 ± 0.53 nd 9.58 43.87 13.4 ± 1.53 21.5 ± 2.15 10.5 ± 1.96 45.4 nd 9.97 ± 0.76 nd 9.97 55.48 24.1 ± 1.51 54.2 ± 3.75 112 ± 9.77 190 nd 6.07 ± 0.36 nd 6.07 1969 19.4 ± 1.20 63.8 ± 3.99 71.4 ± 5.43 155 nd 5.55 ± 0.27 nd 5.55 160

nd: not detected.

Table 2Concentrations (ng-Sn/g) of organotin species in sediments collected along the coast of Hsiao Liouciou Island.

Station No. MBT DBT TBT RBTs MPT DPT TPT RPhTs ROTs

0 15.9 ± 1.90 4.68 ± 0.67 9.69 ± 0.44 30.3 nd nd nd nd 30.31 20.4 ± 1.38 2.83 ± 1.00 5.65 ± 0.23 28.9 nd nd nd nd 28.92 25.8 ± 1.88 3.22 ± 0.21 4.34 ± 0.13 33.4 nd nd nd nd 33.43 36.3 ± 4.02 2.56 ± 0.12 5.33 ± 0.37 44.2 nd nd nd nd 44.24 15.9 ± 0.96 2.44 ± 0.14 3.96 ± 0.84 22.3 nd nd nd nd 22.35 30.0 ± 1.01 2.64 ± 0.11 4.22 ± 0.11 36.9 nd nd nd nd 36.96 14.6 ± 0.87 2.90 ± 0.12 4.05 ± 0.14 21.6 nd nd nd nd 21.67 13.3 ± 1.44 3.10 ± 0.66 4.02 ± 0.73 20.4 nd nd nd nd 20.48 177 ± 19.2 151 ± 9.77 567 ± 19.6 895 nd nd nd nd 8959 56.4 ± 8.90 217 ± 21.1 765 ± 89.2 1038 nd nd nd nd 1038

nd: not detected.

Fig. 2. Percentages of six organotin species (TBT, DBT, MBT, TPhT, DPhT and MPhT) in seawater along the coast of Hsiao Liouciou Island.

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of Taiwan (Hsia and Liu, 2003), probably due to their having beencollected at a significant distance from Pai-Sa and Da-Fu harbors.Also, the boat traffic around Hsiao Liouciou Island is much lowerthan at other harbors of Taiwan, and, as we propose that antifoul-ing paints from ships contribute excess quantities of organotinsinto Taiwan’s waters, less ship traffic could explain these lowerorganotin levels compared to mollusks collected elsewhere in Tai-wan, where shipping traffic tends to be quite high. In fact, onlyabout 1.8 � 104 tons of vessels migrate through the Hsiao Liou-chiou area each year, significantly less than that experienced byan enormous harbor like Kaohsiung (also in southern Taiwan)which experiences about 2.9 � 108 tons of vessels migratingthrough its waters every year.

The concentrations of ROTs in different organs of cobia col-lected at cage mariculture areas ranged between 206 and 859 ng/g (Table 4), with higher concentrations in red muscle, stomach, li-ver, kidney and gonads. The lowest concentrations of RBTs were inabdominal and dorsal muscles, as well as the gills. Fortunately,consumers prefer the former two muscles. These concentrationswere higher than those observed in other fish species collectedfrom waters near Kaohsiung (Hung et al., 1998). This difference

is probably due to differing abilities to concentrate organic pollu-tants in cobia and sea bass, the fish observed by Hung et al.(1998). On the other hand, these concentrations were lower thanthose observed in the same species of cobia collected from an ex-tremely high density cage mariculture area located offshore of Pen-ghu Island, Taiwan, (as high as 53 lg/g, Liu et al., 2006).

Higher percentages of TBT and RBTs relative to other organotinswere observed in both the barnacles Balanus sp. and L. anserifera(67.6 ± 1.39% and 100% for TBT and RBTs, respectively) and cobia(89.4 ± 4.55% and 100%) (Figs. 4 and 5). Also, different percentagesof the six organotin species were found in different fish organs, butTBT was always the highest in all organs. As we mentioned before,butyltins (RBTs) are typically found at higher levels near harborsand cage mariculture area, so we attribute our observations to this.

The general BCF model (Holdway et al., 1983) was used toexamine the accumulation of organotins in R. canadum, Balanussp. and L. anserifera. BCF values for RBTs ranged from 2686 to11199 in cobia and from 4381 to 4654 in L. anserifera and Balanussp. The cobia BCFs were lower than those recorded in cobia fromPenghu Island, Taiwan (as high as 5274, 500, Liu et al., 2006). Thesemay be due to the ship traffic and mariculture cage density being

Fig. 3. Percentages of six organotin species (TBT, DBT, MBT, TPhT, DPhT and MPhT) in sediments along the coast of Hsiao Liouciou Island.

Table 3Concentrations (ng-Sn/g) of organotin species in two barnacle species collected at cage mariculture areas along the coast of Hsiao Liouciou Island.

Species MBT DBT TBT RBTs MPT DPT TPT RPhTs ROTs

Balanus sp. 49.0 ± 6.68 70.4 ± 7.72 238 ± 27.5 357 nd nd nd nd 357Lepas anserifera 42.5 ± 3.56 63.0 ± 7.80 230 ± 33.0 336 nd nd nd nd 336

nd: not detected.

Table 4Concentrations (ng-Sn/g) of organotin species in different tissues of cobia collected at cage mariculture areas along the coast of Hsiao Liouciou Island. ((A) Red muscle; (B)abdominal muscle; (C) dorsal muscle; (D) stomach; (E) gill; (F) liver; (G) kidney; (H) gonads).

Tissues MBT DBT TBT RBTs MPT DPT TPT RPhTs

A 65.7 ± 7.26 33.9 ± 4.10 549 ± 21.3 649 nd nd nd ndB 27.5 ± 3.57 nd 278 ± 37.4 306 nd nd nd ndC 31.5 ± 2.86 nd 394 ± 43.0 425 nd nd nd ndD 28.0 ± 1.43 nd 506 ± 13.6 534 nd nd nd ndE 37.4 ± 3.48 nd 169 ± 19.3 206 nd nd nd ndF 68.6 ± 6.12 39.8 ± 2.79 751 ± 60.5 859 nd nd nd ndG 64.5 ± 9.84 nd 527 ± 45.4 592 nd nd nd ndH 36.0 ± 2.11 nd 545 ± 37.8 581 nd nd nd nd

nd: not detected.

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lower at Hsiao Liouciou Island compared to Penghu Island (Liuet al., 2006).

In summary, organisms located closer to the putative sources oforganotin pollution, Pai-Sa and Da-Fu harbors, possessed higherpercentages of TBT. The results also suggest that the main sourcesof organotin were from Pai-Sa and Da-Fu harbors. Additionally, it ispossible that antifouling paints from the aquaculture cages leachedorganotin compounds into the water.

Acknowledgements

This study was supported by the Republic of China’s NationalScience Council grants NSC 95-2611-M-291-004 and NSC96-2611-M-291-002 to P.-J.M. We sincerely thank Dr. AndersonMayfield for proofreading the final versions of the manuscript.

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Fig. 5. Percentages of six organotin species (TBT, DBT, MBT, TPhT, DPhT and MPhT) in cobia (Rachycentron canadum) at cage mariculture areas along the coast of HsiaoLiouciou Island. (A) Red muscle; (B) abdominal muscle; (C) dorsal muscle; (D) stomach; (E) gill; (F) liver; (G) kidney; (H) gonad.

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