www.elsevier.com/locate/scitotenv

Science of the Total Environm

Toxicity and bioaccumulation of tributyltin and triphenyltin on

oysters and rock shells collected from Taiwan maricuture area

Pei-Jie Menga,T, Jih-Terng Wangb, Li-Lian Liuc, Ming-Hui Chena,c, Tsu-Chang Hungd

aNational Museum of Marine Biology and Aquarium, Biology Department, 2 Houwan Road, Checheng, Pentung, Pingtung 944, TaiwanbTajen Institute of Technology, Ping-Tong 907, Taiwan

cInstitute of Marine Biology, National Sun Yat-sen University, Kaohsiung 804, TaiwandInstitute of Chemistry, Academia Sinica, Taipei 115, Taiwan

Received 30 August 2004; accepted 12 January 2005

Available online 11 March 2005

Abstract

The present study was undertaken to evaluate the toxicity of tributyltin (TBT) on oysters (Crassostrea gigas) and

bioaccumulation of TBT and triphenyltin (TPhT) on oysters and rock shells (Thais clavigera) from mariculture areas of Taiwan.

When treated with concentrations of 0.08, 0.40, 2.00, 10.00 and 50.00 Ag TBT/L, the 48-, 72-, 96- and 120-h LC50s of oysters

were 44.6, 18.4, 17.9 and 14.3 Ag TBT/L, respectively. In the bioaccumulation experiments, oysters and rock shells were exposed

to various concentrations of organotins, i.e. A: control, B: 0.40 Ag TBT/L, C: 0.40 Ag TPhT/L, and D: 0.20 Ag TBT/L + 0.20 AgTPhT/L. In general, TPhT was faster accumulated than TBT in both oysters and rock shells and oysters had a higher

elimination capability than rock shells. Additionally, greater bioaccumulation and elimination rates had been observed in

female oysters than males. To rock shells, the bioaccumulation rate of organotins in imposex females was greater than males

and females.

D 2005 Elsevier B.V. All rights reserved.

Keywords: Bioaccumulation; Organotin compounds; Rock shells and oysters; Sexual phenomena; Hermaproditic/imposex

1. Introduction

Since tributyltin (TBT) was first applied as a moth-

proofing agent in 1925 (Thompson et al., 1985), many

organotin compounds had been produced and used as

biocidal agents, catalysts and stabilizers for polyvinyl

0048-9697/$ - see front matter D 2005 Elsevier B.V. All rights reserved.

doi:10.1016/j.scitotenv.2005.01.016

T Corresponding author. Fax: +8868 8825034.

E-mail address: pjmeng@nmmba.gov.tw (P.-J. Meng).

chloride polymers (Evans and Karpel, 1985). These

compounds such as TBT and triphenyltin (TPhT) have

caused serious pollution problems in coastal areas of

many countries (Meinema et al., 1986; Alzieu, 1989,

1991, 2000; Salazer and Salazer, 1991; Iwata et al.,

1995). Compounds of TBT and TPhT can be degraded

to dibutyltin (DBT), monobutyltin (MBT), diphenyl-

tin (DPhT) and monophenyltin (MPhT), respectively,

by solar radiation, bacterial biodegradation, and/or

biological decomposition (Maguire et al., 1983).

ent 349 (2005) 140–149

P.-J. Meng et al. / Science of the Total Environment 349 (2005) 140–149 141

These compounds are toxic to various marine

organisms especially TBT, for instance, as low as

ppb level in seawater, which can induce oyster shell

abnormalities and spat development failure (Alzieu,

1986, 1991, 2000), imposex on snails (e.g. Wilken et

al., 1994; Fent and Meier, 1994; Horiguchi et al.,

1994; Bryan et al., 1986) and etc.

Although ship related industries contribute

unknown quantities of organotins into the coastal

waters of Taiwan, the Taiwan Agriculture Industry

Association (TAIA, 1997) reported that more than

150 tons of 45% and 20 tons of 2% TPhT acetate

were used for agriculture in 1996 and banned in

2001. Therefore, it is not surprising that as high as

2500 ng/g dry wt of TBT were found in sediments

dredged from the dumpsites in Keelung Harbor

(Hung and Liu, 1998), and high TBT and TPhT (i.e.

1510 and 590 ng/g dry wt, respectively) were

observed in oysters (Crassostrea gigas) from mar-

iculture areas of Shiangsan and Lukang (Hung et al.,

1998). Rock shells (Thais clavigera) in the oyster

0

10

20

30

40

50

60

70

80

90

100

0 20 40 60Hou

0 20 40 60Hour

MO

RT

AL

ITY

(%

)M

OR

TA

LIT

Y (

%)

Fig. 1. The mortality of oysters (C. gigas) expose

mariculture areas with imposex were also observed

(Liu and Suen, 1996; Liu et al., 1997; Hung et al.,

2000, 2001). As expected, the higher the concen-

trations of TBT in rock shells, the higher the

degrees of imposex were found. And, significant

correlations between the length of pseudopenis

versus TBT, DBT, MBT and TPhT were obtained

(Hung et al., 2000). However, most published

studies focused on the acute toxicity and bioaccu-

mulation of TBT and the effects of TPhT on oysters

and snails were still not well understood. Thus, the

current study was undertaken to evaluate the acute

toxicity of TBT on oysters and to compare the

bioaccumulation of TBT and TPhT on oysters and

rock shells simultaneously.

2. Experimental methods

Oysters C. gigas with shell length of 7–10 cm and

rock shells T. clavigera with shell length of 2.5–3.5 cm

80 100 120 140rs

80 100 120 140s

0.08

0.4

2

10

50

0.08

0.4

2

10

50

d to various concentrations of TBT (Ag/L).

Table 1

Concentrations of TBT and TPhT in oysters (C. gigas) and rock shells (T. clavigera) exposed to organotins

Species Sample

size (n)

Sex TBT

(ng/g dry wt)

DBT

(ng/g dry wt)

MBT

(ng/g dry wt)

TPhT

(ng/g dry wt)

DPhT

(ng/g dry wt)

MPhT

(ng/g dry wt)

Before exposure

C. gigas

15 Male 101.9F7.4 ND ND 62.1F26.2 ND ND

15 Female 113F17.7 ND ND 79.6F20.2 ND ND

After exposure for 60 days

A: control 15 Male ND ND 19.5F3.6 ND ND ND

15 Female ND ND ND ND ND ND

B: 0.4 Ag TBT/L 15 Male 537.9F18.2 28.4F7.2 78.2F12.9 ND ND ND

15 Female 686.9F23.9 49.8F12.1 101.9F13.7 ND ND ND

C: 0.4 Ag TPhT/L 15 Male ND ND ND 459.1F12.4 ND ND

15 Female ND ND ND 559.1F26.7 25.8F5.9 ND

D: 0.2 Ag TBT/L +

0.2 Ag TPhT/L

15 Male 138.9F11.5 29.7F14.3 73.1F13.7 215.1F17.4 15.7F5.7 ND

15 Female 218.4F16.8 38.1F6.2 49.8F3.3 312.8F11.9 39.1F8.6 ND

Before exposure

T. clavigera (CK)

15 Male ND ND ND ND ND ND

15 Imposex 59.3F20.2 ND ND 44.9F21.3 ND ND

15 Female 67.0F3.0 ND ND 24.8F3.7 ND ND

After exposure for 73 days

A: control 15 Male ND ND ND ND ND ND

15 Imposex ND ND ND ND ND ND

15 Female ND ND ND ND ND ND

B: 0.4 Ag TBT/L 15 Male 1195.6F25.3 91.3F8.4 ND ND ND ND

15 Imposex 1367.7F19.4 87.1F10.1 48.4F6.7 ND ND ND

15 Female 1357.9F17.6 29.3F9.4 ND ND ND ND

C: 0.4 Ag TPhT/L 15 Male ND ND ND 1569.8F19.7 ND 31.6F5.8

15 Imposex ND ND ND 1629.4F18.3 19.7F6.8 68.3F7.1

15 Female ND ND ND 1507.3F21.8 ND 21.1F5.6

D: 0.2 Ag TBT/L +

0.2 Ag TPhT/L

15 Male 839.5F15.8 69.7F5.4 26.1F7.3 966.5F27.5 37.9F6.8 ND

15 Imposex 788.1F22.4 51.7F5.4 ND 1107.4F13.9 29.4F5.1 ND

15 Female 719.3F17.9 ND ND 1201.9F31.5 ND ND

Before exposure

T. clavigera (SS)

15 Male 69.6F20.5 ND ND 101.9F29.0 ND ND

15 Imposex 108.5F61.8 ND 18.9F6.7 178.9F18.1 ND ND

15 Female 79.6F11.9 ND 17.8F4.3 97.3F21.0 ND ND

After exposure for 73 days

A: control 15 Male ND ND ND ND ND ND

15 Imposex ND ND ND ND ND ND

15 Female ND ND ND ND ND ND

B: 0.4 Ag TBT/L 15 Male 1132.9F23.7 37.1F5.9 ND ND ND ND

15 Imposex 1482.1F25.7 105.7F14.1 23.7F5.8 ND ND ND

15 Female 1379.7F21.9 ND ND ND ND ND

C: 0.4 Ag TPhT/L 15 Male ND ND ND 1609.8F26.7 ND ND

15 Imposex ND ND ND 1718.4F18.9 ND 48.3F6.1

15 Female ND ND ND 1591.8F27.3 ND ND

P.-J. Meng et al. / Science of the Total Environment 349 (2005) 140–149142

Table 1 (continued)

Species Sample

size (n)

Sex TBT

(ng/g dry wt)

DBT

(ng/g dry wt)

MBT

(ng/g dry wt)

TPhT

(ng/g dry wt)

DPhT

(ng/g dry wt)

MPhT

(ng/g dry wt)

After exposure for 73 days

D: 0.2 Ag TBT/L +

0.2 Ag TPhT/L

15 Male 711.8F27.4 39.5F6.6 ND 837.8F47.6 53.2F4.7 19.8F4.3

15 Imposex 795.1F14.2 59.1F8.1 21.7F6.8 1245.5F18.9 ND ND

15 Female 691.2F26.9 ND 37.9F7.9 973.4F34.1 ND ND

A: control; B: 0.4 Ag TBT/L; C: 0.4 Ag TPhT/L; D: 0.2 Ag TBT/L + 0.2 Ag TPhT/L; SS: Shiangsan; CK: Chiku; ND: not detected.

P.-J. Meng et al. / Science of the Total Environment 349 (2005) 140–149 143

were collected from the oyster mariculture areas of

Shiangsan (longitude 24846V02WN, latitude 120854V05WE) and Chiku (Longitude 23803V45WN, latitude

120804V37WE) along the west coast of Taiwan in

August 2000. Immediately after collection, samples

were transported to the Tungkang Marine Laboratory,

Taiwan. Snails and oysters were held separately in

tanks with aerated static seawater at 25 8C and 30x S.

During the cultural and experimental periods, snails

were fed with live oysters and oysters were fed with

microalga (Nannochloropsis sp.) 1% v/v at the density

of 30–50�106 cells/ml, respectively.

A: Y=-1.5573X + 74; p<0.01B: Y=9.622X + 105.86; p<0.005C: Y= -2.1773X + 113.84; p<0.01D: Y=1.9673X + 82.44; p<0.01

0

100

200

300

400

500

600

700

800

0 10 20 30

10 20 30

Da

TB

T(n

g/g)

A B

A B

A: Y=-1.3193X + 65.18; p<0.01B: Y= -1.5473X + 86.58; p<0.01;C: Y=7.206X + 84.36; p<0.005;D: Y=3.928X + 61.28; p<0.005

0

150

300

450

600

0Da

TP

h(ng

/g)

Fig. 2. Accumulation of TBT and TPhT in female oysters (C. gigas) after e

C: 0.4 Ag TPhT/L; and D: 0.2 Ag TBT/L + 0.2 Ag TPhT/L.

Oysters collected from Chiku were used for the

toxicity tests of TBT with the concentrations of 0.08,

0.40, 2.00, 10.00 and 50.00 Ag/L, respectively. Each ofthe experiments was performed twice and 200 oysters

per experiment were reared in aerated static seawater

with 24-h renewed TBT exposures. The lethal con-

centrations for 50% mortality (LC50) of oysters were

determined at hours of 48, 72, 96 and 120. And the

toxicity data were analyzed by the probit analysis.

In the bioaccumulation experiments, oysters and

snails were treated with TBT and TPhT (A, control;

B, 0.40 Ag TBT/L; C, 0.40 Ag TPhT/L; and D, 0.20

40 50 60 70

40 50 60 70

ysC D

C D

ys

xposed to TBT and TPhT for 60 days. A: control; B: 0.4 Ag TBT/L;

P.-J. Meng et al. / Science of the Total Environment 349 (2005) 140–149144

Ag TBT/L + 0.20 Ag TPhT/L) separately. In all the

experiments, 400 oysters or snails per experiment

were reared in aerated static seawater with 24-h

renewed exposures. The concentrations of TBT,

DBT, MBT, TPhT, DPhT and MPhT were determined

in oysters (at day 15, 30, 45, and 60) and snails (at

day 59 and 73). The sex of each sample was

identified as male, female, hermaphrodite or impo-

sex, respectively.

The species of TBT, DBT, MBT, TPhT, DPhT and

MPhT were determined by GC/FPD methods (Hung

et al., 1998). The pooled flesh samples were

extracted with tropolone–benzene solution and the

tetrabutyltin was used as internal standard. The

recovery rates of TBT, DBT, MBT, TPhT, DPhT

and MPhT were 92.4F6.9%, 93.5F8.0%, 85.6F4.0%, 70.4F5.0%, 97.3F10.8% and 75.2F7.0%

(n=3), respectively. Detection limits for TBT, DBT,

MBT, TPhT, DPhT and MPhT were 9.1, 13.4, 8.1,

A: Y=-1.84X + 91.12; p<0.05B: Y=6.846X + 129.68; p<0.01C: Y=-1.644X + 76.82; p<0.05

0

100

200

300

400

500

600

0 10 20 30

0 10 20 30

Da

TB

T(n

g/g)

BA

BA

A: Y=-1.922X + 105.52; p<0.01B: Y=-0.946X + 51.78; p<0.01;C: Y=6.8387X + 72; p<0.005;D: Y=2.9307X + 53.02; p<0.005

0

100

200

300

400

500

600

Da

TP

hT(n

g/g)

Fig. 3. Accumulation of TBT and TPhT in male oysters (C. gigas) after exp

0.4 Ag TPhT/L; and D: 0.2 Ag TBT/L + 0.2 Ag TPhT/L.

15.7, 7.2 and 8.7 ng/g dry wt, respectively. The

accuracy of the analytical methods for TBT was

checked using certified reference biological material

NIES-11 (Leteolabrax japonicus, Cuvier tissue; 1.3F0.1 Ag/g, as chloride). The measured value and

recovery rate for TBT were 1.28F0.05 Ag/g and

98.5% (n=3), respectively. The general linear model

was used to examine the accumulation of organotins

in oysters and snails.

3. Results

3.1. Toxicity of TBT to oysters C. gigas

When treated with 50.00 Ag TBT/L, the mortality

of oysters within 48 h was 100% in the two experi-

ments (Fig. 1). Under the concentrations of 0.08, 0.40,

2.00 10.00 and 50.00 Ag TBT/L, mean values of 48-,

40 50 60 70

40 50 60 70

ysC D

C Dys

osed to TBT and TPhT for 60 days. A: control; B: 0.4 Ag TBT/L; C:

Table 2

The slopes of the bioaccumulation rate (ng/g/day) of TBT and TPhT

in oysters (C. gigas) and rock shells (T. clavigera) treated with

various concentrations of organotins

Species Chemicals Sex A B C D

C. gigas TBT Male �1.84 6.85 �1.64 –

Female �1.56 9.62 �2.18 1.97

TPhT Male �1.92 �0.95 6.84 2.93

Female �1.32 �1.55 7.21 3.93

T. clavigera

(CK)

TBT Male – 17.0 1 11.2

Imposex – – – 9.99

Female – 17.3 – 10.4

TPhT Male – – – –

Imposex – – – –

Female – – 21.1 16.3

T. clavigera

(SS)

TBT Male – 15.0 – 8.97

Imposex – – – 10.1

Female – 18.1 – 8.54

TPhT Male – – – 10.4

Imposex – – – 14.8

Female – – – 12.5

A: control; B: 0.4 Ag TBT/L; C: 0.4 Ag TPhT/L; D: 0.2 Ag TBT/L +

0.2 Ag TPhT/L; CK: Chiku; SS: Shiangsan; –: not correlated.

P.-J. Meng et al. / Science of the Total Environment 349 (2005) 140–149 145

72-, 96- and 120-h LC50s were 44.6, 18.4, 17.9 and

14.3 Ag TBT/L, respectively. In general, the LC50 of

TBT for mariculture oysters decreased as cultural time

increased.

3.2. Bioaccumulation of TBT and TPhT in oysters C.

gigas

Before the bioaccumulation experiments started,

TBT and TPhT had been detected in both female

and male oysters with the concentrations of 102,

113, 62 and 80 ng/g dry wt, respectively (Table

1). After a 60-day exposure to organotins, no

hermaphroditic oysters were observed. By compar-

ison, the control groups had less organotins

accumulated than the groups of prior exposure.

And, in groups of B (0.4 Ag TBT/L) and D (0.2

Ag TBT/L + 0.2 Ag TPhT/L), the final concen-

trations of TBT were 686.9F23.9 and 218.4F16.8

ng/g in females, and 537.9F18.2 and 138.9F11.5

ng/g in males, respectively (Table 1). For groups

C (0.4 Ag TPhT/L) and D (0.2 Ag TBT/L + 0.2

Ag TPhT/L), the final concentrations of TPhT were

559.1F26.7 and 312.8F11.9 ng/g in females, and

459.1F12.4 and 215.1F17.2 ng/g in males, respec-

tively. Bioaccumulation factors for TBT and TPhT

were similar, i.e. in the ranges of 695–1717 and

1075–1564.

In general, the bioaccumulation of TBT and TPhT

in both female and male oysters increased with

cultural time (Figs. 2 and 3). Positive or negative

correlations between cultural time and concentrations

had been observed except on male oysters in the TBT

of group D (Table 2). The steep slopes in high TBT or

TPhT treated groups indicated that bioaccumulation

rates increased as the concentration of medium

increased. By comparing the slopes of TBT and TPhT

in groups D, it is known that different species of

organotins competed with each other during the

accumulation process. And, the accumulation of TPhT

was faster than TBT.

Our data also indicated that oysters could

eliminate organotins when transferred to clean

medium which were shown as the negative slopes

in Table 2. Generally speaking, female oysters

performed higher overall capability of bioaccumula-

tion and elimination of TBT and TPhT than males

(Figs 2 and 3, Table 1).

3.3. Bioaccumulation of TBT and TPhT in rock shells

T. clavigera

Prior to the bioaccumulation experiments, imposex

females had been found in both collection sites, i.e.

Chiku and Shiangsan and organotins had also been

detected on these rock shells (Table 1). The concen-

trations of TBT and TPhT in rock shells from Chiku

were lower than the ones from Shiangsan, such as

ND-67 and 70–109 ng/g for TBT. After a 73-day

exposure to organotins, in groups B (0.4 Ag TBT/L)

and D (0.2 Ag TBT/L + 0.2 Ag TPhT/L), the final

concentrations of TBT in rock shells from Chiku were

1195.6F25.3 and 839.5F15.8 ng/g in males,

1367.7F19.4 and 788.1F22.4 ng/g in imposex

females and 1357.9F17.6 and 719.3F17.9 ng/g in

females, respectively (Table 1). For groups C (0.4 AgTPhT/L) and D (0.2 Ag TBT/L + 0.2 Ag TPhT/L),

the final concentrations of TPhT were 1569.8F19.7

and 966.5F27.5 ng/g in males, 1629.4F18.3 and

1107.4F13.9 ng/g in imposex females and 1507.3F21.8 and 1201.9F31.5 ng/g in females, respectively.

Bioaccumulation factors for TBT and TPhT were in

the ranges of 2989–4198 and 3768–6010. Although

the concentrations in rock shells from Chiku were

lower than the ones from Shiangsan before the

P.-J. Meng et al. / Science of the Total Environment 349 (2005) 140–149146

exposure experiments started, after a 73-day exposure,

the final concentrations of organotins and bio-

accumulation factors from both sites were similar

(Table 1).

The bioaccumulation of TBT and TPhT in rock

shells from both sites increased with cultural time

(Figs. 4 and 5). Positive correlations between cultural

time and concentrations had been observed on most

Chiku (imposex)

0

200

400

600

800

1000

1200

1400

1600

0 20 40 60 80Days

TB

T(n

g/g)

B D

B D

B D

B: Y=18.453X + 104.75D: Y=9.9873X + 45.225; p<0.05

Chiku (female)

0

200

400

600

800

1000

1200

1400

1600

0 20 40 60 80

20 40 60 80

Days

TB

T(n

g/g)

B: Y=17.342X + 61.992; p<0.05D: Y=10.34X + 4.0907; p<0.05

Chiku (male)

0

200

400

600

800

1000

1200

1400

0Days

TB

T(n

g/g)

B: Y=17.043X + 15.092; p<0.05D: Y=11.195X - 6.9336; p<0.05

Fig. 4. Accumulation of TBT and TPhT in rock shells (T. clavigera) coll

control; B: 0.4 Ag TBT/L; C: 0.4 Ag TPhT/L; and D: 0.2 Ag TBT/L + 0.

treatments of D groups (Table 2). The steep slopes in

high TBT or TPhT treated groups indicated that

accumulation rates increased as the concentrations of

medium increased. By comparing the slopes of TBT

and TPhT in group D, it is known that different

species of organotins competed with each other during

the accumulation processes. And, the accumulation of

TPhT was faster than TBT.

Chiku (imposex)

0

200

400

600

800

1000

1200

1400

1600

1800

2000

0 20 40 60 80

20 40 60 80

20 40 60 80

Days

TPh

T(n

g/g)

C D

C D

C D

C: Y=23.164X + 69.232

D: Y=15.255X + 38.393

Chiku (female)

0

200

400

600

800

1000

1200

1400

1600

1800

0Days

TPh

T(n

g/g)

C: Y=21.078X + 9.7674; p<0.05

D: Y=16.277X - 4.2667; p<0.05

Chiku (male)

0

200

400

600

800

1000

1200

1400

1600

1800

0Days

TPh

T(n

g/g)

C: Y=22.425X + 20.921

D: Y=13.71X + 10.685

ected from Chiku after exposed to TBT and TPhT for 73 days. A:

2 Ag TPhT/L.

Shiangsan (imposex)

0

200

400

600

800

1000

1200

1400

1600

1800

0 20 40 60 80

20 40 60 80

Days

TB

T(n

g/g)

B D

B D

B: Y=18.302X + 213.36D: Y=10.13X + 73.687; p<0.05

Shiangsan (female)

0

200

400

600

800

1000

1200

1400

1600

0Days

20 40 60 80

B D

0Days

TB

T(n

g/g)

B: Y=18.052X + 89.689; p<0.05D: Y=8.543X + 83.608; p<0.05

Shiangsan (male)

0

200

400

600

800

1000

1200

1400

TB

T(n

g/g)

B: Y=15.029X + 64.652; p<0.05D: Y=8.9733X + 84.742; p<0.05

Shiangsan (imposex)

0

500

1000

1500

2000

0 20 40 60 80

Days

TPh

T(n

g/g)

C D

0 20 40 60 80

20 40 60 80

DaysC D

DaysC D

C: Y=22.051X + 209D: Y=14.768X + 155.58; p<0.05

Shiangsan (female)

0

500

1000

1500

2000

TPh

T(n

g/g)

C: Y=21.319X + 116.39D: Y=12.537X + 71.957; p<0.05

Shiangsan (male)

0

200

400

600

800

1000

1200

1400

1600

1800

0

TPh

T(n

g/g)

C: Y=20.966X + 162.31D: Y=10.359X + 108.88; p<0.05

Fig. 5. Accumulation of TBT and TPhT in rock shells (T. clavigera) collected from Shiangsan after exposed to TBT and TPhT for 73 days. A:

control; B: 0.4 Ag TBT/L; C: 0.4 Ag TPhT/L; and D: 0.2 Ag TBT/L + 0.2 Ag TPhT/L.

P.-J. Meng et al. / Science of the Total Environment 349 (2005) 140–149 147

Based on the results of group D in Shiangsan, the

capability of bioaccumulation of organotins in impo-

sex females was higher than males and females (Fig.

5, Tables 1 and 2). In addition, rock shells could not

efficiently eliminate organotins as oysters did.

4. Discussion

In the oyster toxicity tests, mean values of 48-, 72-,

96- and 120-h LC50s were 44.6, 18.4, 17.9 and 14.3

Ag TBT/L, respectively. During the accumulation

processes, TPhT was faster accumulated than TBT

in both oysters and rock shells. In addition, oysters

had a higher elimination capability than rock shells. In

oysters, greater bioaccumulation and elimination rates

in females than males had been observed. And, a

higher bioaccumulation rate in imposex rock shells

was also found.

Base on the review by Hall and Pinkney (1985),

adult oysters were reported to be the most resistant

marine organisms to the toxicity of TBT. The 96-h

P.-J. Meng et al. / Science of the Total Environment 349 (2005) 140–149148

LC50s of 210, 290 and 560–1000 Ag/L TBTO were

reported for adult European oysters (Ostreia edulis),

adult Pacific oysters (C. gigas) and adult eastern

oysters (C. virginica). However, our comparable data,

i.e. 17.9 Ag TBT/L, was much lower than those studies.

It is known that environmental factors such as

temperature and salinity affect the tolerance of

organisms in a great extend which may result in

enlarge, narrow, or shift the ranges of the lower or

upper limits (Kinne, 1963). In some species, increas-

ing salinity has been found to increase resistance to

high temperatures, while in others no effect has been

observed. In the studies of fiddler crab zoeae (Uca

pugilator), the 48-h LC50s at 30x S and 10, 20 and

28 8C were 1.4, 0.37 and 0.08 mg trimethyltin/L,

respectively (Hall and Pinkney, 1985). When treated

at 20x S and 10, 20 and 28 8C, the 48-h LC50s were

0.20, 0.04 and 0.03 mg trimethyltin/L, respectively.

As the temperature increased, the values of LC50

decreased accordingly in the case of fiddler crab

zoeae. In the present study, the mean seawater

temperature was 28.5 8C during the experimental

period and a lower tolerance was expected. However,

it cannot be confirmed based on available literatures.

Although the bioaccumulation of organotins by

aquatic organisms has been extensively studied in the

past three decades, available information was mostly

focused on TBT (Laughlin, 1996). The accumulation

factor of TBT in adult oyster C. virginica was 27,800.

In C. gigas, values varied greatly as 2000, 6000, 7000

and 135,000. In the present study, it was from 695 to

1717 and fell into the lower end of reported data. In

the dogwhelk Nucella lapillus, the reported accumu-

lation factors of TBT were 10,000, 10,500 and

100,000 (Laughlin, 1996). The reports that not only

TBT but also TPT promoted imposex in the rock shell

T. clavigera were published by Horiguchi and co-

workers (Horiguchi et al., 1995, 1997a,b, 1998). The

potency of TPT for promoting the development of

imposex in the rock shell is estimated to be

approximately the same as that of TBT (Horiguchi

et al., 1997a). The accumulation factors of TBT and

TPhT have been estimated at 5000–10,000 and

22,000, respectively. These values are much higher

than our results, i.e. 2989–4198 and 3768–6010. It is

known that the relationship between duration of

exposure and occurrence of a steady state is an

important issue in developing a predictive relationship

between exposure and tissue burdens. Thus, the low

accumulation factors of oysters and rock shells found

in our studies may simply result from the failure of

reaching steady states (shown in Figs. 2–5).

In addition, the notable differences between female

and male oysters or imposex females and other rock

shells in bioaccumulation of organotins might be the

reason why the concentrations of TBT and TPhT in

female oysters and imposex rock shells were generally

higher when surveying organotin contents in mar-

iculture areas (Hung et al., 2000, 2001).

Acknowledgements

We are grateful for the constructive comments of

the anonymous reviewers who have substantially

improved the manuscript. This study was supported

by National Science Council/ROC grant NSC89-

2621-B-002-036.

References

Alzieu C. TBT detrimental effects on oysters culture in France—

evolution since antifouling paint regulation. Proceedings of

the Oceans International Organotin Symposium, vol. 4; 1986.

p. 1130–4.

Alzieu C. Monitoring and assessment of butyltins in Atlantic coastal

water. Mar Pollut Bull 1989;20:22–6.

Alzieu C. Environmental problems caused by TBT in France:

assessment, regulation, prospects. Mar Environ Res 1991;

32:7–17.

Alzieu C. Environmental impact of TBT: the French experience. Sci

Tot Environ 2000;258:99–102.

Bryan GW, Gibbs PE, Hummerstone LG, Burt GR. The decline of

the gastropod Nucella lapillus around southwest England:

evidence for the effect of tributyltin from antifouling paint. J

Mar Biol Assoc UK 1986;66:611–40;

Environ 1986;258:99–102.

Evans CJ, Karpel S. Organotin compounds in modern technology. J

Organomet Chem Libr 1985;16:178–217.

Fent K, Meier W. Effects of tributyltin of fish early life stages. Arch

Environ Contam Toxicol 1994;27:224–31.

Hall Jr LW, Pinkney AE. Acute and sublethal effects of organotin

compounds on aquatic biota: an interpretative literature evalua-

tion. CRC Crit Rev Toxicol 1985;14:159–209.

Horiguchi T, Shiraishi H, Shimizu M, Morita M. Imposex and

organotin compounds in Thais clavigera and T bronni in Japan.

J Mar Biol Assoc UK 1994;74:651–69.

Horiguchi T, Shiraishi H, Shimizu M, Yamazaki S, Morita M.

Imposex in Japanese gastropods (Neogastropoda and Mesogas-

P.-J. Meng et al. / Science of the Total Environment 349 (2005) 140–149 149

tropoda): effects of tributyltin and triphenyltin from antifouling

paints. Mar Pollut Bull 1995;31:402–5.

Horiguchi T, Shiraishi H, Shimizu M, Morita M. Imposex in sea

snails, caused by organotin (tributyltin and triphenyltin)

pollution in Japan: a survey. Appl Organomet Chem 1997a;

11:451–5.

Horiguchi T, Shiraishi H, Shimizu M, Morita M. Effects of

triphenyltin chloride and five other organotin compounds on

the development of imposex in the rock shell, Thais clavigera.

Environ Pollut 1997b;95:85–91.

Horiguchi T, Hyeon-Seo C, Shiraishi H, Shibata Y, Soma M, Morita

M, et al. Field studies on imposex and organotin accumulation

in the rock shell, Thais clavigera, from the Seto Inland Sea and

the Sanriku region Japan. Sci Total Environ 1998;214:65–70.

Hung TC, Liu BP. Determination of tributyltin in sediments from

the Machu and Taiwan coastal areas. Acta Oceanogr Taiwanica

1998;37:105–12.

Hung TC, Lee TY, Liao TF. Determination of butyltins and

phenyltins in oysters and fishes from Taiwan coastal waters.

Environ Pollut 1998;102:197–203.

Hung TC, Hsu WK, Meng PJ, Chuang A. Species of organotins in

imposex of rock shells and hermaphroditic oysters from the

western coast of Taiwan. Bull Inst Chem Academia Sinica

2000;47:1–12.

Hung TC, Hsu WK, Meng PJ, Chuang A. Organotins and imposex

in the rock shells, Thais clavigera, from the Taiwan oyster

mariculture area. Environ Pollut 2001;112:145–52.

Iwata H, Tanabe S, Mizuno T, Tatsukawa R. High accumulation of

toxic butyltins in marine mammals from Japanese coastal

waters. Environ Sci Technol 1995;29:2959–62.

Kinne O. The effects of temperature and salinity on marine and

brackish water animals: I. Temperature. Oceanogr Mar Bio Ann

Rev 1963;1:301–40.

Laughlin Jr RB. Bioaccumulation of TBT by aquatic organisms. In:

Champ MA, Seligman PF, editors. Organotin—environmental

fate and effects. London7 Chapman and Hall; 1996.

Liu LL, Suen IJ. Prosobranch gastropod imposex in the west coast

of Taiwan. Venus 1996;55:207–14.

Liu LL, Chen SJ, Peng WY, Hung JJ. Organotin concentrations in

three intertidal neogastropods from the coastal waters of Taiwan.

Environ Pollut 1997;98:113–8.

Maguire RJ, Carey JH, Hale EJ. Degradation of the tributyltin

species in water. J Agric Food Chem 1983;31:1060–5.

Meinema HA, Van Dam-Meerbeek TG, Vonk WJ. Evaluation of

impact of organotin compounds on the aquatic environment.

Final Rept. of TNO, Utrecht to EEC. Contract No. 85/B/600/

11/007/11/N; 1986.

Salazer MH, Salazer SM. Assessing site-specific effects of TBT

contamination with mussel growth rates. Mar Environ Res 1991;

32:131–50.

TAIA. Domestic manufactures production and sale of pesticides in

1996. Taiwan Agriculture Industry Association; 1997.

Thompson JA, Sheffer MG, Pierce RC, Chau YK, Cooney JJ,

Cullen WP, et al. Organotin compounds in the aquatic

environment: scientific criteria for assessing their effects on

environmental quality. National Research Council Canada;

1985. p. 284.

Wilken RD, Kuballa J, Jantzen E. Organotin: their analysis and

assessment in the Elbe river system, north Germany. Fresenius’

J Anal Chem 1994;25:77–84.