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Imposex

From Wikipedia, the free encyclopedia
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]

In species such as 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.[5]

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.[6] 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,[7] but recent studies reported other substances as inducers, such as triphenyltin (TPT)[8] and ethanol.[9] 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.[10]

Affected species

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Main article: List of species affected by imposex

By 1994, imposex had been verified in females of at least 195 gastropod species worldwide.[11] In 2009, this number had sharply increased to a total of 260 species.[12]

Case studies

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Long-term monitoring studies have demonstrated that the prevalence of imposex in marine gastropods is directly correlated with TBT concentrations in the environment. A comprehensive study conducted along the Norwegian coastline from 1991 to 2017 evaluated the levels of TBT and imposex in populations of the dogwhelk (Nucella lapillus).[2] The study documented a significant decline in both TBT concentrations and imposex incidence following the implementation of national and international bans on TBT-based antifouling paints. However, the rate of recovery varied among different localities. This variation was attributed to factors such as sediment characteristics, historical pollution levels, and hydrodynamic conditions, which influence the persistence of TBT in the environment.[2]

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.[13] 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.[14]

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.[15]

Biomonitoring

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Several marine gastropods serve as sensitive bioindicators for assessing TBT pollution through the measurement of imposex levels. The Vas Deferens Sequence Index (VDSI) is a standardized metric employed to quantify the severity of imposex in affected populations. OSPAR utilizes this index to evaluate ecological quality and the success of pollution mitigation strategies.[16] 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.[17]

A study published in 2011 reported that imposex levels are elevated in dog conch (Laevistrombus canarium) populations located near Malaysian ports. However, the researchers found no evidence of sterility among affected females. Their findings suggest that females of L. canarium commonly develop a penis when exposed to organotin compounds in seawater, but this condition does not result in sterility for this species. The dog conch’s ability to tolerate imposex without reproductive failure makes it a reliable local bioindicator for organotin contamination.[18]

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] Nevertheless, while there have been partial recoveries of gastropod populations and a decline in imposex prevalence,[2] several reports have documented persistent imposex cases. 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.[19] Similar situations have emerged involving other species such as Triplofusus giganteus, Strombus pugilis, and Melongena melongena, which indicates that TBT may still linger in sediments or continue to impact large-bodied, long-lived species[15] or rather may still be widely used clandestinely.[20]

See also

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References

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  1. ^ 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 k l 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. ^ 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.
  6. ^ 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.
  7. ^ Ruiz JM, Quintela M, Barreiro R (1998) Tributyltin and imposex: no uncertainty shown. Mar Ecol Prog Ser 170: 293–294
  8. ^ 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.
  9. ^ 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.
  10. ^ 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.
  11. ^ 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.
  12. ^ 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.
  13. ^ Gibbs, Journal of the Marine Biological Association, 1993, vol 73, p 667
  14. ^ Quintela, M; Barreiro, R; Ruiz, J.M (2002). "Dumpton Syndrome reduces the tributyltin (TBT) sterilising effect on Nucella lapillus (L.) by limiting the development of the imposed vas deferens". Marine Environmental Research. 54 (3–5): 657–660. doi:10.1016/s0141-1136(02)00154-x.
  15. ^ a b 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.
  16. ^ Ltd, Michael Carder. "Status and Trends in the Levels of Imposex in Marine Gastropods (TBT in Shellfish)". oap.ospar.org. Convention for the Protection of the Marine Environment of the North-East Atlantic. Retrieved 29 May 2025.
  17. ^ 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.
  18. ^ Cob, Z. C.; Arshad, A.; Bujang, J. S.; Ghaffar, M. A. (2011). "Description and evaluation of imposex in Strombus canarium Linnaeus, 1758 (Gastropoda, Strombidae): a potential bio-indicator of tributyltin pollution" (PDF). Environmental Monitoring and Assessment. 178 (1–4): 393–400. Bibcode:2011EMnAs.178..393C. doi:10.1007/s10661-010-1698-7. PMID 20824325. S2CID 207130813.
  19. ^ 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.
  20. ^ 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.

Further reading

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