Triphenyltin induces imposex in Nucella lapillus through an aphallic route
Introduction
Triphenyltin (TPT) is an organotin compound used until recent years as a fungicide in agriculture in United States and in some countries in Asia (Higley et al., 2013, Yi et al., 2012). For some decades it was also applied as a biocide in ship antifouling systems (AFS), together with the most common organotin biocide at the time—tributyltin (TBT). Both compounds were banned from ship AFS in 2008 through the AFS Convention implemented by the International Maritime Organisation. The leaching of TPT and TBT from ship hulls led to a wide dispersion of these compounds throughout the marine environment, reaching concentrations that could cause adverse effects in biota (Shim et al., 2000, Yi et al., 2012). One of most notable adverse effects is imposex, an endocrine disruption effect defined as the superimposition of male characteristics (penis and vas deferens) in mollusc gastropod females. This phenomenon has been already observed in more than 260 gastropod species worldwide (Titley-O'Neal et al., 2011) and is generally associated to TBT pollution. Although being known that the main causative agent of imposex is TBT, it has been shown in the laboratory that TPT can also induce imposex in the gastropods Reishia clavigera (Horiguchi et al., 1997), Marisa cornuarietis (Schulte-Oehlmann et al., 2000), Nassarius reticulatus (Barroso et al., 2002), Bolinus brandaris (Santos et al., 2006) and Stramonita haemastoma (Limaverde et al., 2007). However, in the dog-whelk Nucella lapillus, one of the most sensitive species to TBT pollution in Atlantic coasts, which has been recommended as a biomonitor by OSPAR (2009), no causative relationship has been obtained until now for TPT and imposex. Moreover, imposex development seems to occur through pathways that involve binding of the agents to nuclear receptors RXR (retinoid X receptor) and PPARγ (peroxisome proliferator-activated receptor gamma) (Castro et al., 2007, Nishikawa et al., 2004, Pascoal et al., 2013). Not only TBT, but also TPT has been shown to be able to bind with high affinity to these receptors (Grun et al., 2006, Kanayama et al., 2005, Nakanishi, 2008). Therefore, since TPT seems to be able to induce in vitro the pathways that may lead to imposex development, we have designed this experiment to understand if TPT is also able to induce imposex in vivo in N. lapillus.
Section snippets
Methods
Dog-whelks were collected from a previously monitored site (Espinho, NW Portugal, 41°00.44N; 8°38.71W), known to have very low imposex levels, with a vas deferens sequence index (VDSI) of 0.4. At the laboratory, specimens were narcotized for a period of 60 min with a solution of 7% MgCl2 in distilled water and analysed under stereomicroscope by gently pulling the gastropod foot out of the shell, to make sex identification possible. Only females not showing signs of imposex were selected for
Results
The mortality during the test ranged between 17% in the control group, which validates the bioassay, and 50% in the highest TPT concentration. Even though the mortality in some experimental groups were high (for instance, 50%), we could still trust the test, because there is no induction of imposex in the control group. Moreover, at least a sample of 15 females per treatment by the end of the exposure period was analysed that guarantees an acceptable number of observations for the statistical
Discussion
Imposex is a phenomenon known to be promoted by TBT and/or TPT. However, only few species are known to develop imposex after exposure to this last compound. Hence, our results add N. lapillus to this list of species, despite other previous studies reporting the opposite (Bryan et al., 1988, Schulte-Oehlmann et al., 2000). Bryan et al. (1988) observed that TPT did not have any effect on imposex promotion in the dog-whelk after exposure via water or injection. However, the initial imposex levels
Acknowledgements
The authors thank the financial support of CESAM (UID/AMB/50017; unit funded by FCT/MEC through national funds, co-funded by the FEDER within the PT2020 Partnership Agreement and Compete 2020 through the project PEst-C/MAR/LA0017/2013) and of the Spanish Ministry of Economy (through the research project IMPACTA, CTM2013-48194-C3). Filipe Laranjeiro and Susana Galante-Oliveira were supported by FCT and POPH/FSE funds through the research grants SFRH/BD/72298/2010 (F.L.) and SFRH/BPD/70368/2010
References (44)
- et al.
Retinoid metabolism in invertebrates: when evolution meets endocrine disruption
Gen. Comp. Endocrinol.
(2014) - et al.
Organotin contamination in the mussel Mytilus galloprovincialis from Portuguese coastal waters
Mar. Pollut. Bull.
(2004) - et al.
Imposex induction is mediated through the Retinoid X Receptor signalling pathway in the neogastropod Nucella lapillus
Aquat. Toxicol.
(2007) - et al.
Development and validation of an OECD reproductive toxicity test guideline with the pond snail Lymnaea stagnalis (Mollusca, Gastropoda)
Regul. Toxicol. Pharmacol.
(2014) - et al.
Long-term temporal trends (1992–2008) of imposex status associated with organotin contamination in the dogwhelk Nucella lapillus along the Icelandic coast
Mar. Pollut. Bull.
(2011) - et al.
Effects of triphenyltin on growth and development of the wood frog (Lithobates sylvaticus)
Aquat. Toxicol.
(2013) - et al.
Spatio-temporal comparisons of imposex status and tissue organotin concentration in the whelk Reishia clavigera collected along the coasts of Dapeng Bay and Daya Bay Shenzhen
China. Mar. Pollut. Bull.
(2014) - et al.
Effects of triphenyltin chloride and five other organotin compounds on the development of imposex in the rock shell, Thais clavigera
Environ. Pollut.
(1997) - et al.
Vas deferens and penis development in the imposex-exhibiting female rock shell, Thais clavigera
Mar. Environ. Res.
(2012) - et al.
Stramonita haemastoma as a bioindicator for organotin contamination in coastal environments
Mar. Environ. Res.
(2007)
Molluscs as multidisciplinary models in environment toxicology
Mar. Pollut. Bull.
Triphenyltin and tributyltin single and in combination, promote imposex in the gastropod Bolinus brandaris
Ecotoxicol. Environ. Saf.
Imposex in the rock shell, Thais clavigera, as evidence of organotin contamination in the marine environment of Korea
Mar. Environ. Res.
Distribution of synthetic organotins and total tin levels in Mytilus galloprovincialis along the Portuguese coast
Mar. Pollut. Bull.
Is aphallic vas deferens development in females related to the distance from organotin sources? A study with Stramonita haemastoma
Ecotoxicol. Environ. Saf.
Review of measured concentrations of triphenyltin compounds in marine ecosystems and meta-analysis of their risks to humans and the environment
Chemosphere
Aphally and imposex in Nucella lapillus from Galicia (NW Spain): incidence, geographical distribution and consequences for the biomonitoring of TBT contamination
Mar. Ecol. Prog. Ser.
The effectiveness of some compounds derived from antifouling paints in promoting imposex in Nassarius reticulatus
J. Mar. Biol. Assoc. U. K.
A comparison of the effectiveness of Tri-N-Butyltin Chloride and five other organotin compounds in promoting the development of imposex in the dog-whelk, Nucella lapillus
J. Mar. Biol. Assoc. U. K.
Variation in foraging behavior among individuals and populations of dogwhelks, Nucella lapillus—natural constraints on energy-intake
J. Anim. Ecol.
Dog-whelks: an introduction to the biology of Nucella lapillus (L.)
Field Stud.
Prosobranch snails as test organisms for the assessment of endocrine active chemicals—an overview and a guideline proposal for a reproduction test with the freshwater mudsnail Potamopyrgus antipodarum
Ecotoxicology
Cited by (20)
Determination of organotin compounds in marine sediments from Arctic Svalbard and West Antarctic Fildes Peninsula
2024, Marine Pollution BulletinAn integrative investigation of developmental toxicities induced by triphenyltin in a larval coral reef fish, Amphiprion ocellaris
2023, Science of the Total EnvironmentToxic effects of triphenyltin on the silkworm Bombyx mori as a lepidopterous insect model
2022, Ecotoxicology and Environmental SafetyThe organotin triphenyltin disrupts cholesterol signaling in mammalian ovarian steroidogenic cells through a combination of LXR and RXR modulation
2022, Toxicology and Applied PharmacologyCitation Excerpt :While TPT can also bind to nuclear receptors, such as RXR, and peroxisome proliferator-activated receptor γ (PPARγ) (Nakanishi, 2008; Harada et al., 2015; Hiromori et al., 2015), little is known regarding its effects on the mammalian ovary. In the context of reproductive function, TPT induces imposex in aquatic species occurs through RXR binding activity (Horiguchi, 2006; Horiguchi et al., 2010; Laranjeiro et al., 2016; Giraud-Billoud and Castro-Vazquez, 2019). In addition, environmentally relevant levels of TPT can significantly suppress aromatase activity in human granulosa-like tumor cells (Saitoh et al., 2001).
Pulsed distribution of organotins in the turbidity maximum zone of the Yangtze Estuary throughout a tidal cycle
2022, Marine Pollution Bulletin