The usefulness of a sediment bioassay with the gastropod Nassarius reticulatus in tributyltin monitoring programs

Highlights

• We performed a sediment bioassay using imposex in gastropods as an endpoint.

• Some sediment samples caused an imposex increase in gastropods.

• Results were compared with imposex levels at the sediment sampling sites.

• The imposex levels variation in 5 years was related with biotest result.

Abstract

Despite the use of tributyltin (TBT) had been banned worldwide in 2008 there is still evidence of its deleterious presence in environment. We evaluate the usefulness of a 28 days sediment bioassay with Nassarius reticulatus females to monitor TBT pollution, using imposex as endpoint. In addition, butyltins were determined in sediments and tissues, and, whenever posible, imposex was assessed in native N. reticulatus at the same sites where sediments were sampled. In the bioassay, a significant increase in imposex parameters was obtained with three sediments (Vi2, Vi3, and Vi4). No correlation was found between this and TBT concentrations in sediment although good correlations were obtained for TBT in tissues, putting in evidence TBT bioavailability in sediment. A significant decrease in imposex from 2008 to 2013 in native snails was only observed at sites that did not cause any effect in the bioassay. In contrast, imposex levels in 2013 were kept as high as 2008 in one of the sites where a significant imposex increase in the bioassay was observed. The bioassay proves thus to be a practical and ecological relevant tool, as: (i) it can be conducted in sites with no native populations of snails, (ii) it provides early identification of polluted sites, anticipating future imposex levels or early identification of recovering, and (iii) it yields information on the bioavailable fraction of the TBT in the sediment. Therefore, this tool can be of extreme usefulness under the scope of recent European legislative frameworks.

Introduction

In order to ensure water quality and prevent hazardous effects observed in aquatic environment, new legislative frameworks have been introduced in Europe, namely Water Framework Directive (WFD) and Marine Strategy Framework Directive (MSDF) (EC, 2000, EC, 2008). These directives demand European Member states to perform effective monitoring plans at ecological and chemical level in order to achieve good ecological status in all water bodies by 2015. One of the compounds listed as a priority substance on WFD’s Annex X is tributyltin (TBT) (Directive 2013/39/EU), considered as the most toxic compound ever released and introduced into the environment (Goldberg, 1986) through its use as biocide in antifouling paints. One of the deleterious effects of TBT is the imposex phenomenon defined as the superimposition of male characters, such as penis and vas deferens, in females of many gastropod species. It was first described by Blaber (1970) in Nucella lapillus and since then this phenomenon was reported in more than 260 gastropods species (Titley-O’Neal et al., 2011) and is globally dispersed (Abidli et al., 2011, Titley-O’Neal et al., 2011, Choi et al., 2013, Cuevas et al., 2014, Lopes-dos-Santos et al., 2014, Paz-Villarraga et al., 2015). In extreme cases imposex can cause female sterility leading to population’s decline, as reported in sites severely contaminated by TBT (Bryan et al., 1986, Gibbs and Bryan, 1996). As a response to these observations, several restrictions on the use of this compound in antifouling paints were applied. In Europe, restrictions on TBT were initially imposed by the directive 89/677/CEE that banned the application of TBT based antifouling paints in small vessels (<25 m) but proved to be inefficient (Barreiro et al., 2001, Barroso and Moreira, 2002, Santos et al., 2002). This, ultimately, led to a global ban on the use of TBT by the IMO International Convention on the Control of Harmful Anti-fouling Systems on Ships that only entered into force in 2008 (IMO, 2001). Previously, European Union introduced Regulation (EC) No 782/2003 that banned the application of organotin antifouling paints on EU boats after 1 July 2003 and forbid its use after 2008 on any boat sailing in European waters.

Seen as the best biomarker for TBT pollution, imposex has been intensively used since the 80s to monitor TBT in marine environment (Bryan et al., 1986, Barreiro et al., 2001, Sousa et al., 2009). It was also considered by OSPAR a mandatory element under the Coordinated Environmental Monitoring Program (CEMP) (OSPAR, 2004) and recently, has been regarded as a useful effect-based tool in monitoring programs under European Frameworks linking chemical and biological elements of quality (EC, 2014). Even with the relevant information obtained from imposex monitoring, this is a phenomenon that may not reflect current TBT levels in the environment as it is an irreversible phenomenon (Gibbs et al., 1987, Oehlmann et al., 1998) and so it can mirror a history of TBT accumulation by the organism throughout life. Therefore, alternative approaches could be used to better assess realistic levels of TBT contamination. Quintela et al. (2000) and Smith et al. (2006) concluded that in situ exposures of N. lapillus with low levels of imposex were highly useful on detecting differences in TBT levels between sites. Rodríguez et al. (2010) found that caging transplant of Nassarius reticulatus, a less sensitive but more ubiquitous species, was also useful in highly contaminated areas. In addition, this species was also responsive to organotin contamination after laboratory exposure to sediment samples collected in the field (Duft et al., 2007). N. reticulatus is considered one of the most reliable gastropod species in Europe for monitoring TBT contamination in sediments (Barroso et al., 2000), and therefore, can be regarded as a good candidate to be used in sediment bioassays. These tests may be adopted in monitoring programs as also pointed out by Oehlmann et al., 2000a, Oehlmann et al., 2000, Duft et al., 2007. Within this perspective, this paper intends to be a further contribution on contamination monitoring efforts under the increasing demands from international institutions, such as OSPAR, ICES or European Union. Moreover, the scientific community identified the use of bioassays and biomarkers in monitoring programs under WFD, as useful tools to complement the information obtained by the assessed quality elements and to investigate the causative agents of a reduced ecological quality status in water bodies (Marín-Guirao et al., 2005, Hagger et al., 2008, Martinez-Haro et al., 2015). Therefore, using Ría de Vigo as a case study, we evaluated the effectiveness of a 28-day sediment bioassay with N. reticulatus, a species with a wide distribution along the North Atlantic in Europe, and compared it with the imposex trends observed in individuals inhabiting the same sites where sediments were collected.