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Villegas, S. ., Iannacone, J. ., & Villegas Galvez, C. G. . (2021). Marine environmental risk due to antifouling paints based on TBT (tributyltin) on “Sea snail” Thaisella chocolata (duclos, 1832) using imposex as a bioindicator, in the port of Paita, Peru. Revista Luna Azul (On Line), (53), 76–91. https://doi.org/10.17151/luaz.2021.53.5
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Authors
Susy Villegas
Perfil Google Scholar
José Iannacone
Carlos Gustavo Villegas Galvez
Abstract
Imposex is the development of male sexual organs in female sea snails by the action of TBT (tributyltin) present in antifouling paints. Objective: to evaluate the environmental risk (ERA) by antifouling paints on Thaisella chocolata (Duclos, 1932) "Sea snail" using imposex as a bioindicator in the port of Paita, Peru. Materials and methods: the imposex indicators of two seasons, summer and spring, were analyzed in four sampling locations; two located in Paita and two in coves further south. A total of 30 individuals of T. chocolata were collected per season, which were narcotized with magnesium chloride. The length of the shell was measured with a Vernier and the soft body was removed. Sex was identified and penis length was measured in males and in females with imposex. The vas deferens index (VDSI) stage was determined. Results: the highest VDSI values between 2.11 (coves) and 3.42 (port of Paita), occurred in the summer season, and the specific ERA for T. chocolata was determined. There are significant differences in the occurrence of imposex in T. chocolata depending on the proximity to the port of Paita, which indicates an environmental risk for this species. Conclusions: the ERA standard for antifouling paints, specific for the species under study, indicates that the environmental risk is between levels C (exposure to TBT in concentrations higher than the Environmental Assessment Criterion) and E (populations unable to reproduce, where most or all females are sterile).
Keywords:
References
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Autoridad Portuaria Nacional (APN). (2018). Estadísticas del movimiento de naves atendidas por la Autoridad Portuaria Nacional a nivel nacional - Reporte RDN02. Autoridad Portuaria Nacional.
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Bech, M. (2002). A survey of imposex in muricids from 1996 to 2000 and identification of optimal indicators of tributyltin contamination along the east coast of Phuket Island, Thailand. Marine Pollution Bulletin, 44, 887–896. https://doi.org/10.1016/s0025-326x(02)00115-7
Braga-Castro, I., Bender-Machado, F., Souza, G.T., Paz-Villarraga, C., & Fillmann, G. (2021). How protected are marine protected areas: A case study of tributyltin in Latin America. Journal of Environmental Management, 278, 111543. https://doi.org/10.1016/j.jenvman.2020.111543
Cacciatore, F., Noventa, S., Antonini, C., Formalewicz, M., Gion, C., Berto, D., ... & Brusà, R. B. (2018). Imposex in Nassarius nitidus (Jeffreys, 1867) as a possible investigative tool to monitor butyltin contamination according to the Water Framework Directive: a case study in the Venice Lagoon (Italy). Ecotoxicology and Environmental Safety, 148, 1078-1089. https://doi.org/10.1016/j.ecoenv.2015.12.039
Cañete, J., Osorio, C., & Huaquín, L. (2015). Nuevos registros de imposex en murícidos de la zona austral de Sudamérica (Estrecho de Magallanes). Revista Ciencia y Tecnología del Mar, 36, 2013-2015.
Carbajal-Enzian, P., Santamaría, J., & Baldárrago, D. (2018). Guía ilustrada para el reconocimiento de poliplacóforos, gasterópodos y cefalópodos con valor comercial en el Perú. Instituto del Mar del Perú (IMARPE).
Castro, I., & Fillman, G. (2012). High tributyltin and imposex levels in the commercial muricid Thais chocolata from two Peruvian harbor areas. Environmental Toxicology and Chemistry, 31, 955-960. https://doi.org/10.1002/etc.1794
Castro, I., Rossato, M., & Fillmann, G. (2012). Imposex reduction and residual butyltin contamination in southern Brazilian harbors. Environmental Toxicology and Chemistry, 31, 947-954. http://dx.doi.org/10.1002/etc.1793
Castro, Í.B., Iannacone, J., Santos, S., & Fillmann, G. (2018). TBT is still a matter of concern in Peru. Chemosphere, 205, 253-259. https://doi.org/10.1016/j.chemosphere.2018.04.097
Chumbimune, L., & Ponce, Z. (2015). Monitoreo de Contaminación por Tributilestaño (TBT) en Puertos de Paracas, Ica (Perú), mediante el fenómeno de Imposex en Stramonita chocolata. Científica, 12, 222-230. https://doi.org/10.21142/cient.v12i3.328
Convention for the Protection of the Marine Environmental (OSPAR). (2008). JAMP Guidelines for Contaminant-Specific Biological Effects. OSPAR Commission. OSPAR convention for the protection of the marine environment of the North-East Atlantic.
Convention for the Protection of the Marine Environmental (OSPAR). (2010). Handbook for the application of Ecological Quality Objectives in the North Sea. Quality Status Report 2010. OSPAR Commission.
Dominguez, D., Patron, O., Nieto, J., Robledo, M., & Velásquez, J. (2015). Imposex en Plicopurpura pansa (Neogastropoda Thaididae) en Nayarit y Sinaloa, México. Revista Mexicana de biodiversidad, 86, 531-534. http://www.redalyc.org/articulo.oa?id=42539890019
El Peruano. (2019, agosto 4). Aprueban la norma para el control de los sistemas antiincrustantes perjudiciales en las naves y artefactos navales de bandera nacional y extranjera que operen en aguas jurisdiccionales peruanas. Resolución directorial Nº RD 477-2019 MGP/DGCG. pp. 12-13. https://busquedas.elperuano.pe/download/url/aprueban-la-norma-para-el-control-de-los-sistemas-antiincrus-resolucion-directoral-no-477-2019-mgpdgcg-1793940-1
Enrique, S., Guabloche, A., Tuesta, E., Iannacone, J., & Castro, I. B. (2019). Imposex responses in Thaisella chocolata and Xanthochorus buxeus from Callao harbor, Peru. Regional Studies in Marine Science, 26, 100510. http://doi.org/10.1016/j.rsma.2019.100510
Fent, K. (1996). Ecotoxicology of organotin compounds. Critical Reviews in Toxicology, 26, 3-117.
França, M.A., Otegui, M.B.P., Zamprogno, G.C., Menario, J.M.F.S., & Costa, M.B. (2021). Imposex and ecological quality status in Stramonita brasiliensis (Claremount &
Reid, 2011): A temporal (2007 to 2018) and spatial evaluation on the southeastern coast of Brazil. Journal of Sea Research, 174, 102080. https://doi.org/10.1016/j.seares.2021.102080
Gibbs, P., Bryan, G., Pascoe, P., & Burt, G. (1987). The use of the dog whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. Journal of the Marine Biological Association of the United Kingdom, 67, 506-523. https://doi.org/10.1017/S0025315400027260
Guabloche, A., Alvarez, J., Rivas, R., Hurtado, S., Pradel, R., & Iannacone, J. (2013). Imposex in the marine snail Xantochorus buxea (Broderip, 1833) (Muricidae) from the South American Pacific. The Biologist (Lima), 11, 237-249. https://dialnet.unirioja.es/servlet/articulo?codigo=4699919
Guabloche, A., Mendoza, J., Minaya, D., Ortega, J., Alvariño, L., & Iannacone, J. (2017). Imposex en el caracol marino Stramonita haemastoma (Gasteropoda: Muricidae) en la costa central del Perú. REDVET. Revista Electrónica de Veterinaria, 18, 1-12. http://www.redalyc.org/articulo.oa?id=63651419006
Hay, M. E. (2009). Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. Annual Review of Marine Science, 1, 193-212. https://doi.org/10.1146/annurev.marine.010908.163708
Mattos, Y. & Romero, M. S. (2016). Imposex in Thaisella chocolata (Duclos, 1832) (Gastropoda: Muricidae) Caldera Bay, Chile. Latin American Journal of Aquatic Research, 44, 825-834. https://doi.org/10.3856/VOL44-ISSUE4-FULLTEXT-18
Moco-Batista, R., Castro, I., & Fillman, G. (2016). Imposex and butyltin contamination still evident in Chile after TBT global ban. Science of the Total Environment, 566, 446-453. https://doi.org/10.1016/j.scitotenv.2016.05.039
International Maritime Organization (IMO). (2000). Application to end by beginning of January 2003 - complete prohibition by January 2008. Propeller, 7, 1-2.
Ministerio de Comercio Exterior y Turismo (MINCETUR). (2016). Isla Foca. http://ficha.sigmincetur.mincetur.gob.pe/index.aspx?cod_Ficha=3047de
Mortaji, H.E., Benhra, A., Elkhiati, N., Haimeur, B.E., Bouhallaoui, M., & Kabine, M. (2020). Imposex induction in Stramonita haemastoma, A bioindicator for organotin contamination in coastal environments. International Journal for Environmental Rehabilitation and Conservation, 9 (SP2), 357-371. https://eoi.citefactor.org/10.11208/essence.20.11.SP2.163
Oehlmann, J., Markert, B., Stroben, E., Schulte-Oehlmann, U., Bauer, B., & Fioroni, P. (1996). Tributyltin biomonitoring using prosobranchs as sentinel organisms. Fresenius' journal of analytical chemistry, 354, 540-545. https://doi.org/10.1007/s0021663540540
Paz-Villarraga, C.A., Castro, Í.B., Miloslavich, P., & Fillmann, G. (2015). Venezuelan Caribbean Sea under the threat of TBT. Chemosphere, 119, 704-710. http://dx.doi.org/10.1016/j.chemosphere.2014.07.068
PRODUCE. (2015). Catrastro acuícola Nacional. Versión 1.0 (febrero 2015). http://catastroacuicola.produce.gob.pe/web/
Qin, L., & Hu, X. (2020). Review of study on Tributyltin-induced Imposex in Gastropods. Advances in Environmental Protection, 10, 269-281. http://dx.doi.org/10.12677/AEP.2020.102031
RLCR. (2004). Aspectos Generales del Convenio de Rotterdam. http://www.fao.org/3/a0137s/a0137s02.htm
Ribeiro-Brasil, D.R.G., Braga-Castro, I., Petracco, M., Moço-Batista, R., Schlemmer-Brasil, L., Azevedo-Ferreira, J., Borba, T.A.C., Rollnic, M., Fillmann, G., & Lund-Amado, L. (2021). Spatial distribution of butyltins and imposex in eastern Brazilian Amazon. Marine Pollution Bulletin, 165, 112155.
Rivas, R., Hurtado, S., Cornelio, D., Mendoza, J., Guabloche, A., Iannacone, J., Alvariño, L., & Castañeda, L. (2017). Imposex en Crassilabrum crassilabrum (Neogastropoda: Muricidae) en la Costa Central del Perú. Revista de Investigaciones Veterinarias del Perú, 28, 834-842. http://www.redalyc.org/articulo.oa?id=371854393007
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. Aquaculture, Aquarium, Conservation & Legislation Bioflux, 12(2), 586-592. http://www.bioflux.com.ro/docs/2019.586-592.pdf
Schøyen, M., Green, N.W., Hjermann, D. Ø., Tveiten, L., Beylich, B., Øxnevad, S., & Beyer, J. (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. https://doi.org/10.1016/j.marenvres.2018.11.011
Smith, B.S. (1971). Sexuality in the American mud snail, Nassarius obsoletus Say. Proceedings of the Malacological Society of London, 39, 377–378. https://doi.org/10.1093/oxfordjournals.mollus.a065117
Spence, S., Hawkins, S., & Santos, R. (1990). The Mollusc Thais haemastoma - An exhibitor of "Imposex" and potential biological indicator of tributyltin pollution. Marine Ecology, 11, 147-156.
Tan, K.S. (1999). Imposex in Thais gradata and Chicoreus capucinus (Mollusca, Neogastropoda, Muricidae) from the straits of Johor: a case study using penis length, area and weight as measures of imposex severity. Marine Pollution Bulletin, 39, 295-303. https://doi.org/10.1016/S0025-326X(98)00181-7
Titley-O'Neal, C.P., Munkittrick. K.R., & Macdonald, B.A. (2011). The effects of organotin on female gastropods. Journal of Environmental Monitoring, 13, 2360-2388. https://doi.org/10.1039/c1em10011d
Vasconcelos, P. (2010). Imposex in Bolinus brandaris from the Ria Formosa lagoon (southern Portugal): Usefulness of single-site baselines for environmental monitoring. Journal Environmental Monitoring, 12, 1823-1832. https://doi.org/10.1039/C0EM00261E
Autoridad Portuaria Nacional (APN). (2018). Estadísticas del movimiento de naves atendidas por la Autoridad Portuaria Nacional a nivel nacional - Reporte RDN02. Autoridad Portuaria Nacional.
Autoridad Portuaria Nacional (APN). (2019). Estadísticas del movimiento de naves atendidas por la Autoridad Portuaria Nacional a nivel nacional -Reporte RDN02. Autoridad Portuaria Nacional.
Bech, M. (2002). A survey of imposex in muricids from 1996 to 2000 and identification of optimal indicators of tributyltin contamination along the east coast of Phuket Island, Thailand. Marine Pollution Bulletin, 44, 887–896. https://doi.org/10.1016/s0025-326x(02)00115-7
Braga-Castro, I., Bender-Machado, F., Souza, G.T., Paz-Villarraga, C., & Fillmann, G. (2021). How protected are marine protected areas: A case study of tributyltin in Latin America. Journal of Environmental Management, 278, 111543. https://doi.org/10.1016/j.jenvman.2020.111543
Cacciatore, F., Noventa, S., Antonini, C., Formalewicz, M., Gion, C., Berto, D., ... & Brusà, R. B. (2018). Imposex in Nassarius nitidus (Jeffreys, 1867) as a possible investigative tool to monitor butyltin contamination according to the Water Framework Directive: a case study in the Venice Lagoon (Italy). Ecotoxicology and Environmental Safety, 148, 1078-1089. https://doi.org/10.1016/j.ecoenv.2015.12.039
Cañete, J., Osorio, C., & Huaquín, L. (2015). Nuevos registros de imposex en murícidos de la zona austral de Sudamérica (Estrecho de Magallanes). Revista Ciencia y Tecnología del Mar, 36, 2013-2015.
Carbajal-Enzian, P., Santamaría, J., & Baldárrago, D. (2018). Guía ilustrada para el reconocimiento de poliplacóforos, gasterópodos y cefalópodos con valor comercial en el Perú. Instituto del Mar del Perú (IMARPE).
Castro, I., & Fillman, G. (2012). High tributyltin and imposex levels in the commercial muricid Thais chocolata from two Peruvian harbor areas. Environmental Toxicology and Chemistry, 31, 955-960. https://doi.org/10.1002/etc.1794
Castro, I., Rossato, M., & Fillmann, G. (2012). Imposex reduction and residual butyltin contamination in southern Brazilian harbors. Environmental Toxicology and Chemistry, 31, 947-954. http://dx.doi.org/10.1002/etc.1793
Castro, Í.B., Iannacone, J., Santos, S., & Fillmann, G. (2018). TBT is still a matter of concern in Peru. Chemosphere, 205, 253-259. https://doi.org/10.1016/j.chemosphere.2018.04.097
Chumbimune, L., & Ponce, Z. (2015). Monitoreo de Contaminación por Tributilestaño (TBT) en Puertos de Paracas, Ica (Perú), mediante el fenómeno de Imposex en Stramonita chocolata. Científica, 12, 222-230. https://doi.org/10.21142/cient.v12i3.328
Convention for the Protection of the Marine Environmental (OSPAR). (2008). JAMP Guidelines for Contaminant-Specific Biological Effects. OSPAR Commission. OSPAR convention for the protection of the marine environment of the North-East Atlantic.
Convention for the Protection of the Marine Environmental (OSPAR). (2010). Handbook for the application of Ecological Quality Objectives in the North Sea. Quality Status Report 2010. OSPAR Commission.
Dominguez, D., Patron, O., Nieto, J., Robledo, M., & Velásquez, J. (2015). Imposex en Plicopurpura pansa (Neogastropoda Thaididae) en Nayarit y Sinaloa, México. Revista Mexicana de biodiversidad, 86, 531-534. http://www.redalyc.org/articulo.oa?id=42539890019
El Peruano. (2019, agosto 4). Aprueban la norma para el control de los sistemas antiincrustantes perjudiciales en las naves y artefactos navales de bandera nacional y extranjera que operen en aguas jurisdiccionales peruanas. Resolución directorial Nº RD 477-2019 MGP/DGCG. pp. 12-13. https://busquedas.elperuano.pe/download/url/aprueban-la-norma-para-el-control-de-los-sistemas-antiincrus-resolucion-directoral-no-477-2019-mgpdgcg-1793940-1
Enrique, S., Guabloche, A., Tuesta, E., Iannacone, J., & Castro, I. B. (2019). Imposex responses in Thaisella chocolata and Xanthochorus buxeus from Callao harbor, Peru. Regional Studies in Marine Science, 26, 100510. http://doi.org/10.1016/j.rsma.2019.100510
Fent, K. (1996). Ecotoxicology of organotin compounds. Critical Reviews in Toxicology, 26, 3-117.
França, M.A., Otegui, M.B.P., Zamprogno, G.C., Menario, J.M.F.S., & Costa, M.B. (2021). Imposex and ecological quality status in Stramonita brasiliensis (Claremount &
Reid, 2011): A temporal (2007 to 2018) and spatial evaluation on the southeastern coast of Brazil. Journal of Sea Research, 174, 102080. https://doi.org/10.1016/j.seares.2021.102080
Gibbs, P., Bryan, G., Pascoe, P., & Burt, G. (1987). The use of the dog whelk, Nucella lapillus, as an indicator of tributyltin (TBT) contamination. Journal of the Marine Biological Association of the United Kingdom, 67, 506-523. https://doi.org/10.1017/S0025315400027260
Guabloche, A., Alvarez, J., Rivas, R., Hurtado, S., Pradel, R., & Iannacone, J. (2013). Imposex in the marine snail Xantochorus buxea (Broderip, 1833) (Muricidae) from the South American Pacific. The Biologist (Lima), 11, 237-249. https://dialnet.unirioja.es/servlet/articulo?codigo=4699919
Guabloche, A., Mendoza, J., Minaya, D., Ortega, J., Alvariño, L., & Iannacone, J. (2017). Imposex en el caracol marino Stramonita haemastoma (Gasteropoda: Muricidae) en la costa central del Perú. REDVET. Revista Electrónica de Veterinaria, 18, 1-12. http://www.redalyc.org/articulo.oa?id=63651419006
Hay, M. E. (2009). Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. Annual Review of Marine Science, 1, 193-212. https://doi.org/10.1146/annurev.marine.010908.163708
Mattos, Y. & Romero, M. S. (2016). Imposex in Thaisella chocolata (Duclos, 1832) (Gastropoda: Muricidae) Caldera Bay, Chile. Latin American Journal of Aquatic Research, 44, 825-834. https://doi.org/10.3856/VOL44-ISSUE4-FULLTEXT-18
Moco-Batista, R., Castro, I., & Fillman, G. (2016). Imposex and butyltin contamination still evident in Chile after TBT global ban. Science of the Total Environment, 566, 446-453. https://doi.org/10.1016/j.scitotenv.2016.05.039
International Maritime Organization (IMO). (2000). Application to end by beginning of January 2003 - complete prohibition by January 2008. Propeller, 7, 1-2.
Ministerio de Comercio Exterior y Turismo (MINCETUR). (2016). Isla Foca. http://ficha.sigmincetur.mincetur.gob.pe/index.aspx?cod_Ficha=3047de
Mortaji, H.E., Benhra, A., Elkhiati, N., Haimeur, B.E., Bouhallaoui, M., & Kabine, M. (2020). Imposex induction in Stramonita haemastoma, A bioindicator for organotin contamination in coastal environments. International Journal for Environmental Rehabilitation and Conservation, 9 (SP2), 357-371. https://eoi.citefactor.org/10.11208/essence.20.11.SP2.163
Oehlmann, J., Markert, B., Stroben, E., Schulte-Oehlmann, U., Bauer, B., & Fioroni, P. (1996). Tributyltin biomonitoring using prosobranchs as sentinel organisms. Fresenius' journal of analytical chemistry, 354, 540-545. https://doi.org/10.1007/s0021663540540
Paz-Villarraga, C.A., Castro, Í.B., Miloslavich, P., & Fillmann, G. (2015). Venezuelan Caribbean Sea under the threat of TBT. Chemosphere, 119, 704-710. http://dx.doi.org/10.1016/j.chemosphere.2014.07.068
PRODUCE. (2015). Catrastro acuícola Nacional. Versión 1.0 (febrero 2015). http://catastroacuicola.produce.gob.pe/web/
Qin, L., & Hu, X. (2020). Review of study on Tributyltin-induced Imposex in Gastropods. Advances in Environmental Protection, 10, 269-281. http://dx.doi.org/10.12677/AEP.2020.102031
RLCR. (2004). Aspectos Generales del Convenio de Rotterdam. http://www.fao.org/3/a0137s/a0137s02.htm
Ribeiro-Brasil, D.R.G., Braga-Castro, I., Petracco, M., Moço-Batista, R., Schlemmer-Brasil, L., Azevedo-Ferreira, J., Borba, T.A.C., Rollnic, M., Fillmann, G., & Lund-Amado, L. (2021). Spatial distribution of butyltins and imposex in eastern Brazilian Amazon. Marine Pollution Bulletin, 165, 112155.
Rivas, R., Hurtado, S., Cornelio, D., Mendoza, J., Guabloche, A., Iannacone, J., Alvariño, L., & Castañeda, L. (2017). Imposex en Crassilabrum crassilabrum (Neogastropoda: Muricidae) en la Costa Central del Perú. Revista de Investigaciones Veterinarias del Perú, 28, 834-842. http://www.redalyc.org/articulo.oa?id=371854393007
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. Aquaculture, Aquarium, Conservation & Legislation Bioflux, 12(2), 586-592. http://www.bioflux.com.ro/docs/2019.586-592.pdf
Schøyen, M., Green, N.W., Hjermann, D. Ø., Tveiten, L., Beylich, B., Øxnevad, S., & Beyer, J. (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. https://doi.org/10.1016/j.marenvres.2018.11.011
Smith, B.S. (1971). Sexuality in the American mud snail, Nassarius obsoletus Say. Proceedings of the Malacological Society of London, 39, 377–378. https://doi.org/10.1093/oxfordjournals.mollus.a065117
Spence, S., Hawkins, S., & Santos, R. (1990). The Mollusc Thais haemastoma - An exhibitor of "Imposex" and potential biological indicator of tributyltin pollution. Marine Ecology, 11, 147-156.
Tan, K.S. (1999). Imposex in Thais gradata and Chicoreus capucinus (Mollusca, Neogastropoda, Muricidae) from the straits of Johor: a case study using penis length, area and weight as measures of imposex severity. Marine Pollution Bulletin, 39, 295-303. https://doi.org/10.1016/S0025-326X(98)00181-7
Titley-O'Neal, C.P., Munkittrick. K.R., & Macdonald, B.A. (2011). The effects of organotin on female gastropods. Journal of Environmental Monitoring, 13, 2360-2388. https://doi.org/10.1039/c1em10011d
Vasconcelos, P. (2010). Imposex in Bolinus brandaris from the Ria Formosa lagoon (southern Portugal): Usefulness of single-site baselines for environmental monitoring. Journal Environmental Monitoring, 12, 1823-1832. https://doi.org/10.1039/C0EM00261E
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