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Imposex

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This female specimen of the queen conch, Aliger gigas, shows signs of imposex: it has developed a male sexual organ (verge) due to previous exposure to organotin compounds.[1]

Imposex is a disorder in sea snails caused by the toxic effects of certain marine pollutants. It is a form of pseudohermaphroditism, where genetically female individuals develop male sexual characteristics, such as a pseudopenis and/or vas deferens, often leading to sterility. Unlike intersex, imposex does not involve gonadal ambiguity but rather a superimposition of male genitalia on otherwise functional female reproductive anatomy.

History

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In the 1950s, organotin compounds were discovered to be highly effective in preventing the buildup of marine organisms on ship hulls, leading to their widespread use in antifouling paints by the 1960s.[2] The use of these paints expanded rapidly during that decade. Around the late 1960s, researchers first observed imposex in the common dogwhelk, Nucella lapillus.[2][3] However, it wasn't until 1981 that this phenomenon was directly linked to organotin exposure.[4] Once the connection was made, pressure mounted to eliminate tributyltin (TBT) and related organotins from marine antifouling products due to their harmful environmental effects.[2]

Biological effects

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Imposex in marine gastropods is triggered by organotin compounds interfering with the hormonal regulation of sexual development. Although this link is well established, scientists have yet to agree on the precise biological mechanisms involved.[2] Several competing theories propose that organotins disrupt different hormonal signaling pathways, including neuroendocrine, steroid-like, or retinoid (vitamin A-related) systems. It is also possible that multiple pathways contribute to the condition, though this has not been definitively confirmed.[2]

Despite uncertainties surrounding the exact mechanisms, a 2006 study identified imposex as one of the few reliable biomarkers for assessing ecological risk and monitoring environmental health.[5] This is due to its high sensitivity, its specificity to organotin exposure, and the relatively well-understood nature of its biological effects. Additionally, imposex is not easily influenced by confounding environmental variables, and the condition in individual snails can be directly linked to broader impacts on population and community dynamics.[2]

Inducing substances

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Tributyltin (TBT) hydride model

Initially, tributyltin (TBT), which can be active in extremely low concentrations, was believed to be the only inducer of imposex,[6] but recent studies reported other substances as inducers, such as triphenyltin (TPT)[7] and ethanol.[8] Tributyltin (TBT) is thought to induce imposex primarily through inappropriate activation of the retinoid X receptor (RXR) pathway. RXR normally plays a role in reproductive development and endocrine signaling in gastropods. TBT acts as a high-affinity ligand for RXR, mimicking endogenous ligands such as 9-cis-retinoic acid, thereby triggering masculinization of female snails.[9]

Affected species

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By 1994, imposex had been verified in females of at least 195 gastropod species worldwide.[10] In 2009, this number had sharply increased to a total of 260 species,[11] including:

Case studies

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In 1993, Scientists from the Plymouth Marine Laboratory found a thriving dog-whelk population in the Dumpton Gap, near Ramsgate in the UK despite high levels of TBT in the water.[27] In the Dumpton Gap population, only 25% of females showed any significant signs of imposex, while 10% of males were characterized by the absence of a penis or an undersized penis, with incomplete development of the vas deferens and prostate. After further experiments, scientists concluded that "Dumpton Syndrome" was a genetic selection caused by high TBT levels. TBT-resistance was improved at the cost of lower reproductive fitness.

In the dog whelk, the growth of a penis in imposex females gradually blocks the oviduct, although ovule production continues. An imposex female dog whelk passes through several stages of penis growth before it becomes unable to maintain a constant production of ovules. Later stages of imposex lead to sterility and the premature death of the females of reproductive age, which can adversely affect the entire population.[26]

In 2024, the first recorded case of imposex in Triplofusus giganteus (the largest marine gastropod in the Atlantic) was reported in Florida. Three out of four wild-collected females exhibited pseudopenis structures, histologically confirmed to contain vas deferens tissue. This discovery was significant given the species’ limited reproductive capacity and ecological importance as a top predator.[24]

Biomonitoring

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Due to their high sensitivity to TBT and other organotin compounds, several gastropod species, such as Nucella lapillus in Europe and Lepsiella scobina in New Zealand, have become established bioindicators for organotin contamination. In the case of L. scobina, the intensity of imposex correlates with environmental TBT levels and has been used to map contamination in coastal waters.[16]

The imposex stages of female dog whelks and other molluscs (including Nucella lima) are used in the United Kingdom and worldwide to monitor levels of tributyltin. The RPSI (Relative Penis Size Index) of females to males, and the VDSI (Vas Deferens Sequence Index) are used to monitor levels of tributyltin in marine environments.

A ban on tributyltin was implemented in Canada in 2003, however, in 2006, dog whelks with imposex could still be found on the shores of Halifax Harbour in Nova Scotia.[28]

Environmental regulations

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Major international organizations, including the Oslo-Paris Commission, the European Commission, and the International Maritime Organization, played crucial roles in driving the global effort to restrict the use of TBT. The first national bans on TBT-based paints for recreational boats and vessels under 25 meters in length were introduced in the late 1980s and early 1990s.[2] Norway implemented this restriction in 1990 and extended it to larger vessels over 25 meters in 2003. A worldwide ban on TBT in all antifouling paints officially came into effect in January 2008. Today, TBT is classified as a priority hazardous substance under both the Water Framework Directive and the Marine Strategy Framework Directive within the European Union.[2]

In the early 1990s, several coastal nations, including Norway, began monitoring TBT levels and the occurrence of imposex in their coastal waters. Not long after the initial bans on TBT-based paints were implemented, snail populations in some of the most heavily impacted areas began to show signs of recovery.[2] Still, while there have been partial recoveries of gastropod populations and a decline in imposex prevalence,[2] persistent imposex cases, such as in Triplofusus giganteus, Strombus pugilis, and Melongena melongena, indicate that TBT may still linger in sediments or continue to impact large-bodied, long-lived species[24] or rather may still be widely used clandestinely.[18]

See also

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References

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  1. ^ a b Voss, Jn; Brown-Peterson, Nj; Delgado, Ga (2025). "Revisiting the imposex queen conch Aliger gigas near Port Everglades, Florida: demographics, histopathology, and sediment contamination". Endangered Species Research. 57: 1–7. doi:10.3354/esr01401.
  2. ^ a b c d e f g h i j Schøyen, Merete; Green, Norman W.; Hjermann, Dag Ø.; Tveiten, Lise; Beylich, Bjørnar; Øxnevad, Sigurd; Beyer, Jonny (2019). "Levels and trends of tributyltin (TBT) and imposex in dogwhelk (Nucella lapillus) along the Norwegian coastline from 1991 to 2017". Marine Environmental Research. 144: 1–8. Bibcode:2019MarER.144....1S. doi:10.1016/j.marenvres.2018.11.011. hdl:11250/2622076. PMID 30497665.
  3. ^ Blaber, Stephen J. M. (1970). "The occurrence of a penis-like outgrowth behind the right tentacle in spent females of Nucella lapillus (L.)". Journal of Molluscan Studies. 39 (2–3): 231–233. doi:10.1093/oxfordjournals.mollus.a065097.
  4. ^ Smith, Blakeman S. (1981). "Male characteristics on female mud snails caused by antifouling bottom paints". Journal of Applied Toxicology. 1 (1): 22–25. doi:10.1002/jat.2550010106. PMID 7185870.
  5. ^ Forbes, Valery E.; Palmqvist, Annemette; Bach, Lis (2006). "The use and misuse of biomarkers in ecotoxicology". Environmental Toxicology and Chemistry. 25 (1): 272–280. Bibcode:2006EnvTC..25..272F. doi:10.1897/05-257R.1. PMID 16494252.
  6. ^ Ruiz JM, Quintela M, Barreiro R (1998) Tributyltin and imposex: no uncertainty shown. Mar Ecol Prog Ser 170: 293–294
  7. ^ Horiguchi, T.; et al. (1995). "Imposex in Japanese gastropods (Neogastropoda and Mesogastropoda): effects of tributyltin and triphenyltin from anti-fouling paints". Marine Pollution Bulletin. 31 (4–12). Oxford: 402–405. Bibcode:1995MarPB..31..402H. doi:10.1016/0025-326X(95)00133-8.
  8. ^ Davies, I. M.; et al. (1997). "Sublethal effects of tributyltin oxide on thedog whelk Nucella lapillus". Marine Ecology Progress Series. 158: 191–204. Bibcode:1997MEPS..158..191D. doi:10.3354/meps158191.
  9. ^ Sternberg, Robin M.; Gooding, Meredith P.; Hotchkiss, Andrew K.; LeBlanc, Gerald A. (2010). "Environmental-endocrine control of reproductive maturation in gastropods: implications for the mechanism of tributyltin-induced imposex in prosobranchs". Ecotoxicology. 19 (1): 4–23. Bibcode:2010Ecotx..19....4S. doi:10.1007/s10646-009-0397-z. PMID 19653098.
  10. ^ a b c Horiguchi, T.; Shiraishi, H.; Shimizu, M.; Morita, M. (1994). "Imposex and organotin compounds in Thais clavigera and T. bronni in Japan". Journal of the Marine Biological Association of the United Kingdom. 74 (3): 651–669. Bibcode:1994JMBUK..74..651H. doi:10.1017/S002531540004772X.
  11. ^ Hiromori, Youhei; Nishikawa, Jun-ichi; Yoshida, Ichiro; Nagase, Hisamitsu; Nakanishi, Tsuyoshi (2009). "Structure-dependent activation of peroxisome proliferator-activated receptor (PPAR) γ by organotin compounds". Chemico-Biological Interactions. 180 (2): 238–244. Bibcode:2009CBI...180..238H. doi:10.1016/j.cbi.2009.03.006. PMID 19497422.
  12. ^ Penchaszadeh, Pablo E.; Antelo, Carlos Sánchez; Zabala, Soledad; Bigatti, Gregorio (2009). "Reproduction and imposex in the edible snail Adelomelon ancilla from northern Patagonia, Argentina". Marine Biology. 156 (9): 1929–1939. Bibcode:2009MarBi.156.1929P. doi:10.1007/s00227-009-1225-y. hdl:11336/95600.
  13. ^ Zou, Yu; Liang, Yuan; Luo, Xuan; You, Weiwei; Shen, Minghui; Fu, Jingqiang; Ke, Caihuan (2025). "Development of a sex-specific molecular marker reveals the ZW/ZZ sex-determination system in Babylonia areolata (link 1807)". Aquaculture. 598: 742044. Bibcode:2025Aquac.59842044Z. doi:10.1016/j.aquaculture.2024.742044.
  14. ^ a b Giulianelli, Sebastián; Ruivo, Raquel; Neuparth, Teresa; Castro, Luís Filipe C.; Bigatti, Gregorio; Santos, Miguel M. (2025). "Cloning and comparative analysis of the retinoid X receptor in two marine gastropods with varying sensitivity to imposex under tributyltin contamination". Environmental Science and Pollution Research. 32 (15): 9479–9488. Bibcode:2025ESPR...32.9479G. doi:10.1007/s11356-025-36278-7. PMID 40128418.
  15. ^ Wells, Fred E.; Keesing, John K.; Gagnon, Marthe Monique; Irvine, Tennille R.; Bessey, Cindy; Spilsbury, Francis (2024). "Annual and decadal surveys of molluscs on intertidal platform reefs in a warming marine environment in the southeastern Indian Ocean provide a baseline for monitoring for future environmental changes". Molluscan Research. 44 (1): 98–106. Bibcode:2024MollR..44...98W. doi:10.1080/13235818.2023.2295778.
  16. ^ a b Stewart, C.; De Mora, S. J.; Jones, M. R.; Miller, M. C. (1992). "Imposex in New Zealand neogastropods". Marine Pollution Bulletin. 24 (4): 204–209. Bibcode:1992MarPB..24..204S. doi:10.1016/0025-326X(92)90531-A.
  17. ^ Costa, M. B.; Zamprogno, G. C.; Pedruzzi, F. C.; Dalbem, G. B.; Tognella, M. M. P. (2013). "Assessing the Continuous Impact of Tributyltin from Antifouling Paints in a Brazilian Mangrove Area Using Intersex in Littoraria angulifera (Lamarck, 1822) as Biomarker". International Journal of Oceanography. 2013: 1–8. doi:10.1155/2013/769415.
  18. ^ a b c d e f Meza-Morelos, Dairo; Johnson Restrepo, Boris; Braga Castro, Ítalo; Fillmann, Gilberto; Fernández Maestre, Roberto (2024). "Imposex incidence in gastropod species from the Colombian Caribbean Coast reveals continued and widespread tributyltin contamination after its global ban". Environmental Pollution. 362: 125010. doi:10.1016/j.envpol.2024.125010. PMID 39313126.
  19. ^ a b c Rumampuk, N. D. C.; Schaduw, J. N. W.; Lintang, R. A. J.; Rompas, R. M. (2019). "Imposex phenomenon in gastropods from Bitung waters, North Sulawesi, Indonesia". AACL Bioflux. 12 (2). ISSN 1844-9166.
  20. ^ Davies, Im; Harding, Mjc; Bailey, Sk; Shanks, Am; Länge, R (1997). "Sublethal effects of tributyltin oxide on the dogwhelk Nucella lapillus". Marine Ecology Progress Series. 158: 191–204. Bibcode:1997MEPS..158..191D. doi:10.3354/meps158191.
  21. ^ Caetano, C. H. S.; Absalão, R. S. (2002). "Imposex in Olivancillaria vesica vesica (Gmelin) (Gastropoda, Olividae) trom a Southeastern Brazilian sandy beach" (PDF). Revista Brasileira de Zoologia. 19 (2). Brazil: Sociedade Brasileira de Zoologia: 215–218. doi:10.1590/S0101-81752002000600022. ISSN 0101-8175.
  22. ^ Abreu, Fiamma E.L.; Lima da Silva, Juliane Natália; Castro, Ítalo Braga; Fillmann, Gilberto (2020). "Are antifouling residues a matter of concern in the largest South American port?". Journal of Hazardous Materials. 398: 122937. Bibcode:2020JHzM..39822937A. doi:10.1016/j.jhazmat.2020.122937. PMID 32768825.
  23. ^ Unger, Michael A.; Harvey, Ellen; Southworth, Melissa; Mann, Roger; Marquardt, Alexandria; Otto, Nathan (2025). "Decreases in TBT concentrations in southern Chesapeake Bay: Evidence for long-term TBT degradation and reduced imposex in the invasive gastropod, Rapana venosa". Marine Pollution Bulletin. 212: 117524. Bibcode:2025MarPB.21217524U. doi:10.1016/j.marpolbul.2024.117524. PMID 39862682.
  24. ^ a b c Leal, José H; Hulse, Carly; D'Agostino, Claire; Fogelson, Susan (2024). "First record of imposex in the horse conch, Triplofusus giganteus (Mollusca: Gastropoda: Fasciolariidae)". Bulletin of Marine Science. 101 (2): 899–900. doi:10.5343/bms.2024.0104.
  25. ^ Barroso, Carlos M.; Rato, Milene; Veríssimo, Alfredo; Sousa, Ana; Santos, José António; Coelho, Sónia; Gaspar, Miguel B.; Maia, Francisco; Galante-Oliveira, Susana (2011). "Combined use of Nassarius reticulatus imposex and statolith age determination for tracking temporal evolution of TBT pollution in the NW Portuguese continental shelf". Journal of Environmental Monitoring. 13 (11): 3018–3025. doi:10.1039/C1EM10508F. PMID 21987262.
  26. ^ a b Castro, Í. B.; et al. (2008). "Imposex in endemic volutid from Northeast Brazil (Mollusca: Gastropoda)" (PDF). Brazilian Archives of Biology and Technology. 51 (5). Brazil: 1065–1069. doi:10.1590/s1516-89132008000500024. ISSN 1516-8913.
  27. ^ Gibbs, Journal of the Marine Biological Association, 1993, vol 73, p 667
  28. ^ Coray, Camille; Bard, Shannon M. (1 May 2007). "Persistence of Tributyltin-Induced Imposex in Dogwhelks (Nucella lapillus) and Intersex in Periwinkles (Littorina littorea) in Atlantic Canada". Water Quality Research Journal. 42 (2): 111–122. Bibcode:2007WQJR...42..111C. doi:10.2166/wqrj.2007.014.
  • Gibbs, P.E., Bryan, G.W. (1986). Reproductive failure in populations of the dog-whelk Nucella lapillus, caused by imposex induced by tributyltin from antifouling paints. J. Mar. Biol. Assoc. U. K. 66: 767–777.
  • "Occurrence of Imposex." Natural Resource Management. 2006.
  • Wirzinger, G., Vogt, C., Bachmann, J., Hasenbank, M., Liers, C., Stark, C., Ziebard, S. & Oehlmann, J. (2007). Imposex of the netted whelk Nassarius reticulatus (Prosobranchia) in Brittany along a transect from a point source. Cah. Biol. Mar. 48(1): 85–94.
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