Tributyltin: A Bottom–Up Regulator of the Crangon crangon Population?

Koen F V Parmentier,Patrick M Roose,Bavo P De Witte,Thierry Burgeot,Stefan Hoffman,Ketil D E Hylland,Guy J Smagghe,Kris Cooreman,Daan H R Delbare,Yves Verhaegen

doi:10.3389/fmars.2019.00633

Abstract

The restrictions and the concerted action of the global ban on the use and presence of tributyltin (TBT) in marine applications to protect ecosystems in the marine environment in 2008 was mainly based on the economic impact on shellfish industries and the dramatic extinction of local mollusc populations in the past. In contrast to the vast datasets on effects on molluscs, the knowledge on impacts on species from other taxa remained in the uncertain until almost two decades ago. The assumption on a long-term TBT-mediated pernicious metabolic bottom-up regulation of the crustacean Crangon crangon population was provoked by the outcome of an EU-project ‘Sources, Consumer Exposure and Risks of Organotin Contamination in Seafood’. This study reported high TBT body burdens in C. crangon in 2003, at the start of the transition period to the global ban. Experimental research on the TBT impact in C. crangon focused on agonistic interference with natural ecdysteroid hormones at the metabolic pathways regulating growth and reproduction and the biogeochemical distribution of the chemical. In this paper, metabolic, topical and population-relevant biological endpoints in C. crangon and other crustaceans are evaluated in relation to the temporal and spatial trends on TBT’s occurrence and distribution in the field during and after the introduction of the tributyltin restrictions and endocrine-related incidents. Arguments are forwarded to relate the German Bight incident on growth and reproduction failure in the C. crangon population, despite the lack of direct evidence, to the pernicious impact of tributyltin in 1990/91 and previous years. The extreme occurrence of TBT in C. crangon from other parts of the southern North Sea and evidence on the high body burdens as dose metrics of exposure also feeds the suspicion on detrimental impacts in those areas. This paper further demonstrates the complexity of distinguishing and assessing the individual roles of unrelated stressors on a population in an integrated evaluation at the ecosystem level.

Highlights

It is in the meantime known that TBT-mediated endocrine disruption and imposex/intersex developments in the sensitive gastropods Nucella lapillus, Nassarius reticulatus (= Hinia reticulata) and other mollusks are related to TBT’s agonistic interference with the growth- and reproduction nuclear receptor (NR) retinoid-X and its ecdysteroid hormone triggers (Nishikawa et al, 2004; Sousa et al, 2010; Sternberg et al, 2010)
Attention tochronic TBT toxicity in crustaceans was long not an issue of particular interest due to the initial moderate lethal toxicity compared to mollusks, and C. crangon’s long-term non-endangered status
Most assessments on TBT impact on organisms in the marine environment were based on water exposure toxicity correlations between effects and TBT levels in water

Summary

INTRODUCTION

The application of the broad-spectrum organotin biocide tributyltin as antifouling agent (Figure 1) since the mid-1900s was economically a success until, at the end of the 1970s, fertility and calcification impairments on oysters and induction of imposex and intersex in female snails linked TBT to the decline and local extinction of many mollusk species (Smith, 1981; Alzieu et al, 1982; Bryan et al, 1986, 1989; Gibbs et al, 1987; Waldock et al, 1988; Mensink et al, 1996a; Ide et al, 1997; Oehlmann et al, 1998, 2007). Acute 96 h-LC50 values of 28.5–41 μg TBT oxide (TBTO)/l did not draw up a particular sensitivity of Abbreviations: 9-cis RA, 9-cis-retinoic acid; AFS, Convention on the Control of Harmful Antifouling Systems of IMO; BCF, bioconcentration factor; BSAF, biota to sediment accumulation factor; cDNA, copy- or complement-DNA; CrcEcR, C. crangon ecdysteroid receptor; CrcRXR, C. crangon retinoid X-receptor; DBT, dibutyltin; Dw, dry weight; ECHA, European Chemicals Agency; EcR, ecdysteroid receptor; EFSA, European Food Safety Authority; EU, European Union; ICES, International Council for the Exploration of the Sea; IMO, International Maritime Organization; Kow, Octanol-Water Partition Coefficient; LC50, median lethal concentration; LOEC, Lowest Observed Effect Concentration; LPUE, Landings per Unit Effort; MBT, monobutyltin; MEPC, Marine Environment Protection Committee of IMO; NOEC, No Observed Effect Concentration; NR, nuclear receptor; OT, organotin; OT-SAFE, Sources, consumer exposure and risks to organotins (OTs) accumulated in seafood; pHi, Intracellular pH; pKa, Acid-dissociation constant; RXR, retinoid-X-receptor; SSD, Species Sensitive Distribution; TBT, tributyltin; TBTO, Bis(tributyl)tin oxide. We refer to, among other (Evans et al, 1996; Fent, 1996; Champ, 2000; Birchenough et al, 2002; Stronckhorst and van Hattum, 2003; Antizar-Ladislao, 2008; Morton, 2009; Oliveira et al, 2009; Rodríguez et al, 2009; Sousa et al, 2009; Bengtsson and Wernersson, 2012; Sunday et al, 2012; Matthiessen, 2013; Wetzel et al, 2013; OSPAR, 2014; Langston et al, 2015; Nicolaus and Barry, 2015; Wilson et al, 2015; Schøyen et al, 2018)

TBT LEVELS IN THE SOUTHERN NORTH SEA

MECHANISM OF ACTION OF TBT IN CRUSTACEANS

KNOWLEDGE GAPS

CONCLUSION

Findings

AUTHOR CONTRIBUTIONS