AbstractImposex is the development of male features in female prosobranch gastropods, caused by organotin compounds. In the Mexican Pacific coast, imposex was observed in Plicopurpura pansa. This snail has been used by indigenous people to dye cotton and traditional fabric clothing. During 2010 and 2011, 5 habitats were visited along the coastline of Nayarit and Sinaloa, Mexico. At low tide, 675 snails were collected. Shell length, sex ratio and imposex incidence were measured. Imposex incidences were higher in the samples collected near harbor areas

Domínguez-Ojeda, Delia

Nieto-Navarro, José Trinidad

Patrón-Soberano, Olga Araceli

Robledo-Marenco, María de Lourdes

Velázquez-Fernández, Jesús Bernardino

Revista Mexicana de Biodiversidad

Elsevier - Publisher Connector 

Imposex in Plicopurpura pansa (Neogastropoda: Thaididae) in Nayarit and Sinaloa, Mexico 

Imposex is the development of male features in female prosobranch gastropods, caused by organotin compounds. In the Mexican Pacific coast, imposex was observed in Plicopurpura pansa. This snail has been used by indigenous people to dye cotton and traditional fabric clothing. During 2010 and 2011, 5 habitats were visited along the coastline of Nayarit and Sinaloa, Mexico. At low tide, 675 snails were collected. Shell length, sex ratio and imposex incidence were measured. Imposex incidences were higher in the samples collected near harbor areas

Delia Domínguez-Ojeda

Olga Araceli Patrón-Soberano

José Trinidad Nieto-Navarro

María de Lourdes Robledo-Marenco

Jesús Bernardino Velázquez-Fernández

Directory of Open Access Journals

cAi2sACKREt6rDbPmM1CAvailable online at www.sciencedirect.comRevista Mexicana de Biodiversidadwww.ib.unam.mx/revista/Revista Mexicana de Biodiversidad 86 (2015) 531–534Research noteImposex in Plicopurpura pansa (Neogastropoda: Thaididae) in Nayaritand Sinaloa, MexicoImposex en Plicopurpura pansa (Neogastropoda: Thaididae) en Nayarit and Sinaloa, MéxicoDelia Domínguez-Ojeda a, Olga Araceli Patrón-Soberano b, José Trinidad Nieto-Navarro a,∗,María de Lourdes Robledo-Marenco c, Jesús Bernardino Velázquez-Fernández ca Escuela Nacional de Ingeniería Pesquera, Universidad Autónoma de Nayarit, Bahía de Matanchén km 12, carretera a Los Cocos, 63740, San Blas, Nayarit,Mexicob División de Biología Molecular, Instituto Potosino de Investigación Científica y Tecnológica, Camino a la presa de San José, Núm. 2055, Lomas 4ta, Sección,78216 San Luís Potosí, MexicoLaboratorio de Contaminación y Toxicología Ambiental, Universidad Autónoma de Nayarit, Ciudad de la Cultura Amado Nervo, S/N, Los Fresnos, 63155, Tepic,Nayarit, MexicoReceived 25 June 2014; accepted 10 February 2015Available online 26 May 2015bstractImposex is the development of male features in female prosobranch gastropods, caused by organotin compounds. In the Mexican Pacific coast,mposex was observed in Plicopurpura pansa. This snail has been used by indigenous people to dye cotton and traditional fabric clothing. During010 and 2011, 5 habitats were visited along the coastline of Nayarit and Sinaloa, Mexico. At low tide, 675 snails were collected. Shell length,ex ratio and imposex incidence were measured. Imposex incidences were higher in the samples collected near harbor areas.ll Rights Reserved © 2015 Universidad Nacional Autónoma de México, Instituto de Biología. This is an open access item distributed under thereative Commons CC License BY-NC-ND 4.0.eywords: Organotin compounds; Endocrine disruptionesumenEl imposex es el desarrollo de características masculinas en hembras de gasterópodos prosobranquios, causado por compuestos organoestañosos.n la costa del Pacífico mexicano se observó el imposex en el caracol Plicopurpura pansa. Este caracol ha sido utilizado por grupos indígenas paraeñir algodón y fabricar su ropa tradicional. Durante 2010 y 2011, se visitaron 5 hábitats en la costa de Nayarit y Sinaloa, México. Se recolectaron75 caracoles durante la marea baja; se midió la longitud de la concha, proporción de sexos y la incidencia de imposex. De acuerdo con losesultados, la incidencia de imposex fue más alta en las muestras recolectadas en las áreas cercanas a los muelles.erechos Reservados © 2015 Universidad Nacional Autónoma de México, Instituto de Biología. Este es un artículo de acceso abierto distribuidoajo los términos de la Licencia Creative Commons CC BY-NC-ND 4.0.alabras clave: Compuestos organoestañosos; Disrupción endocrinae(The organotin compounds (OTC’s) are considered a threat toarine life in areas with intense maritime activities and can act as∗ Corresponding author.E-mail address: nieto@uan.edu.mx (J.T. Nieto-Navarro).Peer Review under the responsibility of Universidad Nacional Autónoma deéxico.ODGeihttp://dx.doi.org/10.1016/j.rmb.2015.04.018870-3453/All Rights Reserved © 2015 Universidad Nacional Autónoma de México,ommons CC License BY-NC-ND 4.0.ndocrine disruptors in marine invertebrates, mainly gastropodsAxiak, Micallef, Muscat, Vella, & Mintoff, 2003; Fioroni,ehlmann, & Stroben, 1991; Gagné, Blaise, Pellerin, Pelletier,ouville, M., Gauthier-Clerc, S. et al., 2003; Matthiessen, &ibbs, 1998). One of the most studied toxic effects of OTC’s onndocrine disruption in gastropods is imposex, which consistsn the imposition of male sexual characters, like penis andInstituto de Biología. This is an open access item distributed under the Creative532 D. Domínguez-Ojeda et al. / Revista Mexicana de Biodiversidad 86 (2015) 531–53423.52322.52221.521106,5 106 105,5Isabel IslandMonasSanta CruzChacalaOcasoMazatlán (Olas Altas)Pacific Ocean NayaritSinaloaFMvSSotDoUP(PA(TpiIMCi(izfPSwo(iiitIisdbnfF(g5swith this characteristic were examined under a stereomicroscopeand all showed albumen and capsule glands, characteristic offemales (Gibbs, & Bryan, 1994). Imposexed females found atigure 1. Sampling sites in Nayarit and Sinaloa in the Pacific coast. Ocaso,onas, Santa Cruz and Chacala in Nayarit; Olas Altas in Sinaloa.as deferens in females (Gibbs, & Bryan, 1987; Horiguchi,hiraishi-Shimizu, & Morita, 1994; Mensink et al., 2002;mith, 1981). Imposex is a widespread phenomenon known toccur in more than 190 species of marine gastropods throughouthe world (Pessoa, Fernandez, Toste, Dores, & Parahyba, 2009).ue to its high sensitivity, imposex has been used as a biomarkerf TBT contamination in several coastal countries such as thenited Kingdom (Bryan, Burt, Gibbs, & Pascoe, 1993; Gibbs,ascoe, & Burt, 1988), Japan (Horiguchi et al., 1994), CanadaTester, & Ellis, 1995), Australia (Gibson, & Wilson, 2003),atagonia (Bigatti & Penchaszadeh, 2005), Brazil (Castro,lves De Lima, Braga, & Rocha-Barreira, 2007), MalaysiaMohamat et al., 2010) and Mexico (Rodríguez-Romero, 2010).his study represents the first published report on Plicopurpuraansa; this species is an intertidal carnivorous gastropod, whichnhabits rocky intertidal beaches exposed to strong wave action.t is distributed in the Pacific Ocean from the northwesternexican coast (Keen, 1971) to northern Peru (Paredes, Huamán,ardoso, Vivar, & Vera, 1999; Peña, 1970) and has been used byndigenous people to dye cotton and traditional fabric clothingTurok et al., 1988). In this study, a higher incidence of imposexn areas close to human settlements was observed.Regions with high human activity are expected to renderones with higher pollution levels than regions farther awayrom human settlements. Keeping this in mind, 5 habitats of. pansa along the Pacific coastline of Mexico (Nayarit andinaloa states) with different proximity to human settlementsere chosen (Fig. 1). In order to define the sampling area, a linef 50 m long parallel to the coast with 2 m width was studied.According to the criterion of Stephenson and Stephenson1949), the sampling was carried out in the mid-littoral andFaFigure 2. Male characteristics in P. pansa.nfra-littoral fringe, collecting all the specimens in the area dur-ng 2010 and 2011. The shell length, sex ratio (male:female) andmposex incidence (I%) within the population were obtained;hen afterward, individuals were returned to the habitats.mposex incidence was estimated through the percentage ofmposex females in each site, using the following equation:I% =(Number of females with imposexTotal number of females)× 100Data were analyzed using software Sigmastat 3.5®. Chi-quare (p = 0.05) was used to determine significant statisticalifferences between sampling stations and imposex levels.P. pansa males were identified by the penis, which is locatedehind the right cephalic tentacle, a common feature amongeogastropods. This organ has a characteristic inverted-cedilleorm with 2-mm width becoming thicker at the base (Fig. 2).emales were identified due to (1) the absence of a penis, and2) the presence of organs such as the albumen gland and capsuleland (Fig. 3).The female penis appears as a nub structure, no longer thanmm and no wider than 2 mm (Fig. 4). Thus, snails with a nubtructure were considered as imposexed females. Ten femalesigure 3. Female anatomy of P. pansa in ventral view. Dg: digestive gland, Ag:lbumen gland, Cg: capsule gland, Gon: gonad.D. Domínguez-Ojeda et al. / Revista Mexicana de Biodiversidad 86 (2015) 531–534 533Figure 4. (A) Imposexed female of P. pansa from Ocaso; (B) imposexed female of P. pansa from Olas Altas. Pseudopenis or imposex are marked with an arrow.Table 1Imposex quantification in Plicopurpura pansa at the sampling sites. Data presented as mean ± SD. SL: shell length; T: total snails collected; M: male; NF: normalfemales; IF: imposexed females; TF: total females; SR: sex ratio; I%: imposex percentage.Sampling sites SL (cm) T M NF IF TF (NF+IF) SR (M:F) I%Olas Altas 3.63 ± 0.54 170 81 64 25 89 0.91 28.1Santa Cruz 3.17 ± 0.40 99 52 37 10 47 1.11 21.3Las Monas 3.90 ± 0.87 89 40 47 2 49 0.82 4.1El Ocaso 2.71 ± 0.72 280 149 130 1 131 1.14 0.8Chacala 2.70 ± 0.48 75 37 38 0 38 0.97 0.0tsnialwflog(esmDhFttfI21ci2Pmaatewhe 4 sites showed no vas deferens and their penises were alwaysmaller than those of the males.Imposex incidences were higher in the samples collectedear harbor areas (Table 1). The highest percentage occurredn Olas Altas, the nearest site to the harbor in Sinaloa, with highnthropogenic activities with 28.1% of affected females, fol-owed by Santa Cruz, the nearest site to the harbor in Nayaritith 21.3%. According to the chi-square test, significant dif-erences were observed in the percentages of imposex betweenocations (p < 0.05) (Fig. 5).In the study area, the size range of imposex affected femalesscillated between 2.8 and 5.8 cm length. Evidence to date sug-ests that imposex is generally caused by tributyltin (TBT)Davies, Harding, Bailey, Shanks, & Lange, 1997; Garaventat al., 2008; Minchin, 2003; Smith, 1981), a chemical mas-ively used in antifouling paints, which until recently was theost effective solution to prevent fouling on boat hulls (Terlizzi,elos, Garaventa, Faimali, & Geraci, 2004). Several studiesave linked imposex in neogastropods with TBT contamination40353025Percentage of imposex %20151050Olas Altas Santa Cruz Monas∗∗ ∗Ocaso Chacalaigure 5. Percentage of imposex in Plicopurpura pansa of 5 study sites. *Sta-istically different with respect to Olas Altas and Santa Cruz. p < 0.05 Chi squareest.ndTtiltfMoeaaUsFrom antifouling paint in the marine environment (DeFur, Crane,ngersoll, & Rattersfield, 1999; Jenner, 1979; Li, & Collin,009; Ramón, & Amor, 2001; Short, Rice, Brodersen, & Stickle,989).Despite the reduced percentage of imposex in the study areaompared with other regions in North, Central and South Amer-ca (Miloslavich, Penchaszadeh, & Bigatti, 2007; Pessoa et al.,009; Tester, & Ellis, 1995), in the present study, imposex in. pansa could be due to the presence of OTC’s in the environ-ent. Monitoring results suggest that harbors in the samplingrea are the probable source of OTC pollution, demonstrated bytendency of increased imposex levels in sampling points nearhe harbors.OTC pollution is a major concern to the health of aquaticnvironments by the International Maritime Organization (IMO)hich proposed a worldwide OTC ban, but the prohibition hasot yet come into effect in many developing countries (Lousada,os Santos, Castro, & Fillmann, 2013; Pessoa et al., 2009).herefore, it is extremely important to control organotin con-amination in order to review the enforcement of IMO rulingsn Mexico. Although the sites chosen for this study showed lowevels of imposex, Mexico needs to develop a monitoring policyo protect its coasts.This is the first report of imposex in P. pansa in Mexico, buturther research determining OTC dispersal would be valuable.onitoring of the OTC’s and the use of gastropods as sentinelrganisms (Oehlmann et al., 1996) could be a useful tool forstablishing the extent of OTC pollution on Mexican coasts,long with an analysis of the chemical composition of both waternd sediments.We thank Posgrado Ciencias Biológico Agropecuarias,niversidad Autónoma de Nayarit. This research was made pos-ible through grants NAYARIT 2008-C01-93389, supported byomix-Nayarit.5 xicanRABBCDDFGGGGGGHJKLLMMMMMOPPPRRSSSTT34 D. Domínguez-Ojeda et al. / Revista Meeferencesxiak, V., Micallef, D., Muscat, J., Vella, A., & Mintoff, B. (2003). Imposexas a biomonitoring tool for marine pollution by tributyltin: Some furtherobservations. Environment International, 28, 743–749.igatti, G., & Penchaszadeh, P. E. (2005). Imposex in Odontocymbiola mag-ellanica (Caenogastropoda: Volutidae) in Patagonia. Comunicaciones de laSociedad Malacológica del Uruguay, 88, 371–375.ryan, G. W., Burt, G. R., Gibbs, P. E., & Pascoe, P. L. (1993). Nassarius reticu-latus (Nassariidae: Gastropoda) as an indicator of tributyltin pollution beforeand after TBT restrictions. Journal of the Marine Biological Association ofthe United Kingdom, 73, 913–929.astro, I. B., Alves De Lima, A. F., Braga, A. R. C., & Rocha-Barreira, C. A.(2007). Imposex in two muricid species (Mollusca: Gastropoda) from thenortheastern Brazilian Coast. Journal of the Brazilian Society of Ecotoxicol-ogy, 2, 81–91.avies, I. M., Harding, M. J. C., Bailey, S. K., Shanks, A. M., & Lange, R. (1997).Sublethal effects of tributyltin oxide on the dog whelk Nucella lapillus.Marine Ecology Progress Series, 158, 191–240.eFur, P. L., Crane, M., Ingersoll, C. G., & Rattersfield, C. J. (1999).Endocrine disruption in invertebrates: endocrinology, testing and assess-ment. Pansacola, Florida: Society of Environmental Toxicology andChemistry (SETAC).ioroni, P., Oehlmann, J., & Stroben, E. (1991). The pseudohermaphroditism ofProsobranchs: Morphological aspects. Zoologischer Anzeiger, 226, 1–26.agné, F., Blaise, C. C., Pellerin, J., Pelletier, E., Douville, M., Gauthier-Clerc,S., et al. (2003). Sex alteration in soft-shell clams (Mya arenaria) in anintertidal zone of the Saint Lawrence River (Quebec, Canada). ComparativeBiochemistry and Physiology, Part C, 134, 189–198.araventa, F., Centanni, E., Fioroni, S., Noventa, S., Terlizzi, A., Faimalli, M.,et al. (2008). New implications in the use of imposex as suitable tool fortributyltin contamination: Experimental induction in Hexaplex trunculus(Gastropoda: Muricidae) with different stressors. Cell Biology and Toxi-cology, 24, 563–571.ibbs, P. E., & Bryan, G. W. (1987). TBT paints and demises of the dog-whelkNucella lapillus (Gastropoda). Journal of the Marine Biological Associationof the United Kingdom, 68, 1482–1487.ibbs, P. E., & Bryan, G. W. (1994). Biomonitoring of tributyltin (TBT) pollutionusing the imposex response of neogastropod molluscs. In J. Kess, & M.Kramer (Eds.), Biomonitoring of coastal waters and estuaries (pp. 205–226).Boca Ratón: CRC Press.ibbs, P. E., Pascoe, R. L., & Burt, G. R. (1988). Sex change in the femaledogwhelk, Nucella lapillus, induced by tributyltin from antifouling paints.Journal of the Marine Biological Association of the United Kingdom, 68,715–731.ibson, C. P., & Wilson, S. P. (2003). Imposex still evident in eastern Australia10 years after tributyltin restrictions. Marine Environmental Research, 55,101–112.origuchi, T., Shiraishi-Shimizu, H. M., & Morita, M. (1994). Imposex andorganotin compounds in Thais clavigera and Thais bronni in Japan. 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Imposex in Plicopurpura pansa (Neogastropoda: Thaididae) in Nayarit and Sinaloa, Mexico

"Imposex is the development of male features in female prosobranch gastropods, caused by organotin compounds. In the Mexican Pacific coast, imposex was observed in Plicopurpura pansa . This snail has been used by indigenous people to dye cotton and traditional fabric clothing. During 2010 and 2011, 5 habitats were visited along the coastline of Nayarit and Sinaloa, Mexico. At low tide, 675 snails were collected. Shell length, sex ratio and imposex incidence were measured. Imposex incidences were higher in the samples collected near harbor areas.""El imposex es el desarrollo de características masculinas en hembras de gasterópodos prosobranquios, causado por compuestos organoestañosos. En la costa del Pacífico mexicano se observó el imposex en el caracol Plicopurpura pansa . Este caracol ha sido utilizado por grupos indígenas para teñir algodón y fabricar su ropa tradicional. Durante 2010 y 2011, se visitaron 5 hábitats en la costa de Nayarit y Sinaloa, México. Se recolectaron 675 caracoles durante la marea baja; se midió la longitud de la concha, proporción de sexos y la incidencia de imposex. De acuerdo con los resultados, la incidencia de imposex fue más alta en las muestras recolectadas en las áreas cercanas a los muelles.

Domínguez Ojeda, Delia

Patrón Soberano, Olga Araceli

Nieto Navarro, José Trinidad

Robledo Marenco, Maria De Lourdes

Velázquez Fernández, Jesús Bernardino

Repositorio IPICYT

Imposex en Plicopurpura pansa (Neogastropoda: Thaididae) en Nayarit y Sinaloa, México

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Imposex in Plicopurpura pansa (Neogastropoda: Thaididae) in Nayarit and Sinaloa, Mexico

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