SPECIAL ISSUE: INDICATORS OF OCEAN POLLUTION
Imposex in Reishia clavigera as an Indicator to Assess Recovery
of TBT Pollution After a Total Ban in South Korea
Nam Sook Kim
Sang Hee Hong
Won Joon Shim
Received: 29 June 2016 / Accepted: 17 January 2017 / Published online: 20 May 2017
Ó Springer Science+Business Media New York 2017
Abstract The temporal changes in the frequency and
degree of imposex and tributyltin (TBT) levels in gas-
tropod (Reishia clavigera) were evaluated in Jinhae Bay, 5
and 10 years after the total ban on TBT usage in South
Korea. The frequency and degree of imposex decreased
signiﬁcantly after the ban, accompanied by an increase in
the female-to-male ratio. The TBT concentrations in R.
clavigera also decreased signiﬁcantly after the ban. There
were good correlations between the TBT concentration in
rock shell and both the degree of imposex and the female-
to-male ratio. The total TBT ban effectively reduced the
TBT levels and the frequency and degree of imposex in R.
clavigera. However, the current low exposure level in the
study area is still sufﬁcient to cause imposex in R. clav-
igera. More time is needed to reduce the TBT levels to
levels that do not have adverse biological effects on R.
The organotin compound tributyltin (TBT) was used widely
as a biocide in antifouling paint to prevent organisms from
settling on vessel hulls for over four decades before its
regulation. The TBT in antifouling paint on ship hulls was
designed to be released into the surrounding water, where it
caused unintended adverse biological effects on nontarget
marine organisms. Several adverse biological effects have
been reported since the 1980s, including endocrine pertur-
bations in gastropods (Abidli et al. 2012). One of the most
detrimental effects of TBT on aquatic biota was imposex
(i.e., the development of male sexual organs in females) with
impaired reproductive function in female gastropods.
Imposex in female gastropods is a sensitive, very speciﬁc
biomarker and indicator of TBT pollution in the marine
environment (Shim et al. 2000; Chan et al. 2008; Qiu et al.
2011; Laranjeiro et al. 2015).
Based on toxic effects of TBT on nontarget marine
species, many countries prohibited the use of TBT in the
mid 1980s and early 1990s (Champ 2000; Sonak et al.
2009). The use of TBT in Korea was ﬁrst regulated in
2000, and it was banned completely in 2003 (Shim et al.
2005; Kim et al. 2008; Choi et al. 2009). The Anti-
Fouling System Treaty of the International Maritime
Organization banned the use of triorganotin-based paint
on ships in 2008 (IMO 2008). Consequently, the TBT
levels in seawater and biota have declined in many areas
since the introduction of these regulations (Sousa et al.
2007; Choi et al. 2009; Lahbib et al. 2011; Verhaegen
et al. 2012; Kim et al. 2014; Wilson et al. 2015). Nev-
ertheless, TBT is still detected in many coastal regions
(Rodriguez et al. 2009; Paz-Villarraga et al. 2015), and
sedimentary TBT levels worldwide have declined either
slowly or have remained unchanged following bans on
TBT (Diez et al. 2002; Kim et al. 2014).
The monitoring of imposex in gastropods and TBT
contamination is still necessary, despite the decrease in
TBT concentration in seawater following its ban. TBT is
detectable in coastal environments and imposex is induced
& Won Joon Shim
Oil and POPs Research Group, Korea Institute of Ocean
Science and Technology, Geoje 53201, Republic of Korea
Department of Marine Sciences and Convergent Technology,
Hanyang University, Ansan 15588, Republic of Korea
Department of Marine Environmental Sciences, Korea
University of Science and Technology, Daejeon 34113,
Republic of Korea
Arch Environ Contam Toxicol (2017) 73:301–309