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Ecotoxicology and Environmental Safety
journal homepage: www.elsevier.com/locate/ecoenv
Imposex levels and butyltin compounds (BTs) in Hexaplex trunculus
(Linnaeus, 1758) from the northern Adriatic Sea (Italy): Ecological risk
assessment before and after the ban
Federica Cacciatore
a,⁎
, Rossella Boscolo Brusà
a
, Seta Noventa
a
, Camilla Antonini
a
,
Vanessa Moschino
b
, Malgorzata Formalewicz
a
, Claudia Gion
a
, Daniela Berto
a
,
Massimo Gabellini
c
, Maria Gabriella Marin
d
a
ISPRA - Institute for Environmental Protection and Research, Loc. Brondolo, 30015 Chioggia Venice, Italy
b
CNR, ISMAR, Arsenale Tesa, 104, Castello 2737-F, 30122 Venice, Italy
c
ISPRA - Institute for Environmental Protection and Research, via Vitaliano Brancati, 48, Rome, Italy
d
University of Study of Padua, Department of Biology, Via U. Bassi, 58/B, 35131 Padua, Italy
ARTICLE INFO
Keywords:
Vas Deference Sequence Index
Relative Penis Size Index
Bioaccumulation
Water Framework Directive
Ecological Quality Ratio
Venice Lagoon
ABSTRACT
The aim of this study was to compare imposex and butyltin compounds (BTs) data, collected before and after the
organotin ban in 2008, in order to assess temporal and spatial variation of the phenomenon, the decline of BT
contamination, and the effects on Hexaplex trunculus population in the coastal area of the northern Adriatic Sea,
close to the Venice Lagoon. Both in marine and in lagoon sites, the results obtained in 2013–2015 showed a
significant decline in the incidence of imposex in respect to those from the 2002 survey. In 2002, lagoon samples
exhibited Relative Penis Size Index (RPSI) higher than marine samples, whereas no differences were detected in
the recent survey, when all RPSI values were below 0.6%. Vas Deference Sequence Index (VDSI) mean values
were over 4 before the ban introduction and below this value after that, indicating more critical conditions for
gastropod population in 2002 rather than in 2013-15. Percentage of sterile females was up to 69% in 2002,
whilst in the more recent survey no sterile female was found. Range of BT concentrations in gastropods de-
creased from 252 to 579 to 16–31 ng∑BT/g d.w. BT body burdens varied according to a gender dependant
pattern, with higher concentrations observed in females than in males. A first attempt to propose a classification
based on BT impact on H. trunculus, according to the Water Framework Directive, revealed that most sites were
in Bad ecological status before the ban and attained a Poor/Moderate status after that.
1. Introduction
Imposex is a phenomenon described for the first time by Smith
(1971), which consists of the superimposition of male sexual characters
onto female gonochoristic gastropods. It is one of the most studied ef-
fect of tributyltin (TBT) which affected more than 260 species of gas-
tropods, and it is used as TBT specific biomarker all over the world,
mostly in those species which have shown a significant correlation
between the degree of morphological alterations and the concentrations
of the contaminant (Titley-O′Neal et al., 2011). In most of caenogas-
tropoda species, imposex can lead to population decline as a con-
sequence of sterility and reproduction failure (Bryan et al., 1986).
Among these species, Hexaplex trunculus (Linnaeus, 1758) has been
used as a bioindicator of butyltin (BT) pollution in Mediterranean areas,
such as along the coasts of Malta (Axiak et al., 1995, 2000, 2012),
Tunisia (Lahbib et al., 2008, 2009, 2011; Anastasiou et al., 2016),
Croatia (Garaventa et al., 2006, 2007; Carić et al., 2016; Erdelez et al.,
2017) and Italy (Terlizzi et al., 1998, 1999, 2003; Chiavarini et al.,
2003; Pellizzato et al., 2004; Garaventa et al., 2006, 2007; Anastasiou
et al., 2016), both before and after the TBT global ban adopted in 2001
by the International Convention on the control of harmful antifouling
systems on ships (AFS-Convention 2001). The global ban came into
force in September 2008 (IMO, 2001), but in the European Union it was
enacted by the EC Regulation 782/2003 which totally interdicted the
application of organotin compounds on ships after 1st of July 2003 and
forced the eradication of these compounds from ships from 1st January
2008 (EC, 2003). These regulations arose from evidences of organotin
high toxicity to many aquatic organisms and significant long-term
ecological impacts at very low concentrations on non-target marine
species (Axiak et al., 2012). Due to their persistence, toxicity and
http://dx.doi.org/10.1016/j.ecoenv.2017.09.027
Received 17 May 2017; Received in revised form 7 September 2017; Accepted 11 September 2017
⁎
Corresponding author.
E-mail address: federica.cacciatore@isprambiente.it (F. Cacciatore).
Ecotoxicology and Environmental Safety 147 (2018) 688–698
0147-6513/ © 2017 Elsevier Inc. All rights reserved.
MARK