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Imposex in Thaisella chocolata (Duelos, 1832) (Gastropoda: Muricidae) Caldera Bay, Chile.

Imposex en Thaisella chocolata (Duclos, 1832) (Gastropoda: Muricidae) de Bahia Caldera, Chile


Anthropogenic pollution has severe effects on the biology of marine organisms (Collado et al., 2010). One example is the so-called imposex syndrome, defined by Smith (1971) as the superimposition of nonfunctional male sex organs in the female genital system of gastropods. In extreme cases, imposex prevents the normal reproduction of specimens and can even cause death and extinction of affected female populations (Oehlmann et al., 1991). This virilizing alteration is induced by the organotin compound called TBT (tributyltin), used as a biocide in antifouling paints and other products (Castro et al., 2012).

The extent of anatomical malformations is dependent on the concentration of TBT in the environment (Gibbs & Bryan, 1986) and can range from mild, forming a pseudopenis primordium to very severe obstruction of the gonoduct (Oberdorster & McClellan-Green, 2002). Various scales and indices have been developed to standardize the stages of imposex that consider mainly the degree of development of the cephalic structures (pseudopenis and vas deferens) and occlusion of the vagina (Gibbs et al., 1987; Fioroni et al., 1991; Oehlmann et al., 1991; Stroben et al., 1992; Barreiro et al., 2001; Fernandez et al., 2002; Rodriguez et al., 2008). A few scales use microscopic alterations associated with imposex (Oehlmann et al., 1991; Schulte-Oehlmann et al., 1997; Huaquin et al., 2004; Horiguchi et al., 2014).

Determining the occurrence and severity of the syndrome is particularly important in commercial species, since these are subjected regularly to fishing mortality. In addition, the edible species should be studied due to the potential effects of TBT on human health, including impaired immune system, altered response to physiological stimuli (IPCS, 1990), promoting of adipogenesis (Bernardes et al., 2013) and even it is also suspected to act as a carcinogen (Y amabe et al., 2000; Nakanishi, 2007).

Thaisella chocolata (Duclos, 1832) is a gastropod extracted for human consumption (Avendano et al., 1998) and represents a significant benthic resource species for the artisanal fisheries sector in northern Chile; however, due to high levels of exploitation since the beginning of its extraction in 1978, with a maximum of 8,244 ton in 1986 (Avendano et al., 1998), protective measures that included the establishment of a minimum capture size of 5.5 cm and a fishing ban for one or two years was decreed by region (Avendano et al., 1998). Currently, this species is extracted in the north and in the south of Chile; in 2015 total landings were 492 ton (SERNAPESCA, 2015).

Anatomical observations on females of T. chocolata from Caldera Bay, Atacama Region, led us to hypothesize the imposex occurrence in this species. In that locality a number of productive activities are performed, that includes the shipment of mineral concentrates, fuel discharge, artisanal and industrial fisheries, aquaculture and tourism (Castillo & Valdes, 2011).

In order to determine the occurrence and intensity of imposex in female of T. chocolata from Caldera Bay, this study characterizes the anatomical and histopathological abnormalities of the female reproductive system and estimates the proportion, grades and indices of imposex. To propose T. chocolata as a sentinel species, different scales of imposex were applied to determine the scale that best fits the alterations observed in this species, including the scales of Gibbs et al. (1987), Stroben et al. (1992), Barreiro et al. (2001), Fernandez et al. (2002) and Rodriguez et al. (2008).


One hundred and eighty individuals of T. chocolata were collected by hookah diving in Caldera Bay (27[degrees]2'47"S, 70[degrees]49'29"W), Atacama Region, Chile, from down to 16 m depth, on February 2012. Live specimens were transferred to the wet laboratory of the North Catholic University, Coquimbo, where they were kept in 200 L aquaria with circulating seawater and continuous aeration for five days until analysis. For each specimen we recorded the maximum length of the shell with a vernier with 0.01 mm accuracy. The maximum length of the penis of males and the pseudopenis of females were measured from the base of the body to the distal end using the Image Pro-Plus program. Soft tissue was extracted by breaking the shell and sex was determined by biopsy of the gonad observed in vivo in a photonic microscope Olympus CX31 with magnification 40x to 1000x.

Females were classified with imposex observing the ovarian, albumen, ingestive and capsule glands, vagina, vas deferens, pseudopenis and penis duct of males and females. Photograph of these organs were taken with a camera Nikon FX 35A. Transverse and longitudinal sections of the organs previously named were extracted. The sections were observed and described under a stereoscopic microscope Nikon SMZ-10 in order to clarify their delimitation with other structures and location of the gonoduct.

Additionally, a linear regression was performed to establish the effect of the Average Pseudopenis/Penis Length (APL), using as covariate Average Shell Length (ASL) between males (n = 90) and females (n = 90) of the same locality. Subsequently, by an analysis of co-variance (ANCOVA) the effect of these variables was established. Normality of the data was determined using the Kolmogorov-Smirnov and Lilliefors tests and homogeneity by the Levene test. Significant differences between treatments (male and females) were detected by ANDEVA.

The histopathological alterations of the female system affected by imposex were analyzed in 20 females. From each female we obtained cross sections of 0.5 [cm.sup.3] of ovary, glands, oviduct and vagina. The tissue pieces were fixed in Davidson's fixative for 24 h and processed according to the standard technique described by Martoja & Martoja-Pierson (1970). Sections 5 pm thick were stained with Harris hematoxylin and eosin, and then mounted with Flotexx[R] resin. The preparations were observed with a magnification 40x to 1000x and photographed in a light microscope equipped with an Olympus CX31 UCMAD3 camera. Measurements of organs and histological structures were performed using the Image ProPlus program.

The proportion of females affected was estimated in 90 specimens through the following formula: I% = (number of females with imposex/total number of females)x100 (Gibbs et al., 1987). The progress of imposex was determined by applying the scale of Gibbs et al. (1987) and indices of imposex of Gibbs were estimated as follows: Vas Deferens Stages Index (VDSI) = ([SIGMA] of degrees of VDS/total number of females analyzed), Relative Penis Length Index (RPLI) = (average pseudopenis length in females/average penis length in males)x100 and Relative Penis Size Index (RPSI) = (average pseudopenis length in females /average penis length in males)3x100 (Gibbs et al., 1987). We also applied the scales of Stroben et al. (1992); Barreiro et al. (2001); Fernandez et al. (2002) and Rodriguez et al. (2008), who consider the development of vas deferens, pseudopenis, the convolution of the oviduct and the occurrence of aborted ovicapsules.


Anatomical and histopathological alterations

The 90 females of T. chocolata, sex corroborated by gonadal histological analysis, had prostate gland tissue in the mantle cavity, a pseudopenis and vas deferens at different levels of development. The female reproductive system of T. chocolata from Caldera Bay fits the characterization of imposex, which consist, from anterior to posterior, of a pseudopenis, penile duct, vas deferens, vagina, capsule, ingestive and albumen glands, seminal receptacle, oviduct and an ovary.

The pseudopenis is located on the right tentacle of the specimens; it is of sigmoidal shape and has a filiform extension at its end corresponding to a filament (Fig. 1a). Other abnormalities were detected in the head region of two specimens. In one, two pseudopenises are originated from the same base on the right tentacle (Fig. 1b); one measured 0.8 cm and the other 0.5 cm in length. In a second specimen there was a dense round structure located on the vas deferens. It was pigmented pinkish brown with white spots and measured 1 cm length (Fig. 1c). Moreover, in this individual the anterior and posterior ends of pseudopenis were fused by their epidermis (Fig. 1c).

The epidermis of the pseudopenis is similar to that of the head and foot of the specimen and is formed by ciliated columnar cells interspersed with mucous cells. Underlying the epidermis are muscle cells of circular, longitudinal and diagonal arrangement. The pseudopenis contains a closed, narrow and pleat lumen penis duct. The conduit consists of ciliated columnar epithelium and is closely surrounded by a thick and compact layer of circular muscle and connective tissue (Fig. 2a). The male conduit has a large lumen surrounded by a layer of circular muscle (Fig. 2b).

For females there was a positive correlation between the ASL (x axis) and the APL (y axis) (ANCOVA, n = 90; r = 0.7; P < 0.05) (Fig. 3). Besides, it was determined that the length of the pseudopenis of females (n = 90; ASL: 83.9 [+ or -] 11.1 mm and APL: 10.6 [+ or -] 2.0 mm; P < 0.05) was significantly less than the penis of males (n = 90; ASL: 82.8 [+ or -] 9.5 mm and APL: 17.8 [+ or -] 2.4 mm; P < 0.05).

The vagina is in the anteroventral end of the mantle cavity (Fig. 4a). The vulva is a shallow oval slot due to melting of the muscular walls of the vagina. In three of ten specimens, the vulva was occluded and instead shows a thin red line corresponding to the vas deferens, which concludes in the base of the pseudopenis and extends posteriorly to the muscular region of the vagina (Fig. 4a). On the outskirts of the vagina are located prostate gland acini (Fig. 4b).

The capsule gland is tubular and thinned at its anterior end. It is cream color and often has a nodular appearance on its surface (Fig. 5a). 16% of females contained compacted ovicapsules inside the gland, forming a brown solid sphere (Fig. 5b), which includes mucus mass, yolk granules and irregular fragments of fibrous sheets similar to layers of ovicapsules.The walls of the gland tend to be laminar, organized into two lateral lobes and the posterior lobe not distinguished. The gland measured on average 2.1 [+ or -] 0.5 cm in length (n = 10). The epithelium of the gonoduct has sections of different thickness and metaplastic appearance ranging from cylindrical to cuboidal cells (Fig. 5c). The organization of the glandular tissue is interrupted by acellular areas with homogeneous appearance and low dye affinity (Fig. 5d). Cell clusters were detected in scattered regions of the gland with pyknotic nuclei (Fig. 5e) and in the periphery of the gland are acini of prostate gland (Fig. 5f).

The ingestive gland is formed by numerous dark brown color saccules composed of cylindrical epithelium cells and granular cytoplasm. On the outskirts of this gland are located acini of the prostate gland (Fig. 6). Only six of ten specimens had an ingestive gland.

The albumen gland is located on the ventral right side, prior to the kidney. It is tubular in shape, curved in its dorsal end and cream color. It measures on average 0.5 [+ or -] 0.3 cm in length (n = 10). It consists of two side lobes, delimited by a ciliated columnar epithelium with oval and basal nuclei. In some sections the epithelium is modified like a pseudostratified epithelium (Fig. 7a) and lacks basal lamina (Fig. 7b). The demarcation between albumen and capsule glands is diffuse (Fig. 7c) and the acini of the prostate gland are located interspersed between the peripheral acini of the albumen gland (Fig. 7d).

The seminal receptacle corresponds to tubules located in a dorsal position between the albumen and ingestive glands. It consists of a cubic and simple epithelium surrounded by a layer of circular muscle.

The apical portion of the epithelial cells has spermatozoids adhered by their heads with their flagella directed towards the lumen. The seminal receptacle was present in three specimens of the ten analyzed.

The oviduct arises from the ovary and travels through the body as a straight tube of white color, internally lined by a cylindrical simple and ciliated epithelium, surrounded by a thick layer of circular muscle and connective tissue.The ovary is attached to the surface of the digestive gland. The color varies from cream to yellow-cream, according to the state of maturity. It is organized on elongated tubules composed of a germinal epithelium from which the previtellogenic and vitellogenic oocytes originate.

Proportion and degrees of imposex

All females of T. chocolata examined (n = 90) from Caldera Bay possessed a pseudopenis and vas deferens, which indicates that a high proportion suffers from imposex (I% = 100%). In the five scales applied, the largest proportion of females with imposex was classified in the higher grades, except for that of Barreiro et al. (2001) (Table 1).

In the scales of Gibbs et al. (1987) and Fernandez et al. (2002), on average 81% of females of T. chocolata examined had a vermiform structure called pseudopenis and a continuous vas deferens, followed by 19% females with ovicapsules aborted in the lumen of the capsule gland, corresponding to the last grade in the scale of Rodriguez et al. (2008) (Table 1).

In addition to the superimposition of these two male organs and the occurrence of aborted ovicapsules in the female system of T. chocolata there were other anomalies, particularly in the vagina, considered by the scale of Stroben et al. (1992). In this scale, 48% of the analyzed females showed a reduction in the size of the vulva, nodules in the vaginal opening and/or the presence of prostatic tissue in the vaginal muscles, as well as the occurrence of a penis duct in the other 40% (Table 1). The VDSI index of imposex was 4.8 and the values of the other female indices were: RPLI = 59.6 and RPSI = 21.8


Anatomical and histopathological alterations

The most drastic anatomical and histological alterations identified in this study occur in the vagina and the reproductive glands. Occlusion of the vagina and its replacement by the vas deferens are the main cause of infertility in females. In addition, the capsule, ingestive and albumen glands are reduced in size and/or missing compared to females without imposex. This condition may prevent the normal production of secretory material used in packaging oocytes (Huaquin et al., 2004) and in providing intracapsular material. Notable was the occurrence of ovicapsular materials and traces of yolk inside the capsule gland even when no presence of spermatozoids was recorded anywhere in the reproductive tract in these specimens. This suggests that females with imposex try to reproduce with still-unfertilized oocytes. The most revealing histological evidence of the extreme degree of virilization that females with imposex suffer is the presence of prostatic acini interposed in the vagina tissue and surrounding the reproductive glands.

The mechanisms underlying the masculinization and development of imposex have not been fully elucidated. One of the currently most accepted hypothesis ssuggests an activation induced by TBT on retinoid X receptors (RXR), normally present in the reproductive organs and the cephalic region (Urushitani et al., 2013; Horiguchi et al., 2014).

In Caldera Bay there are no measurements of TBT in the environment, however, this locality is characterized by the development of productive activities that involve the presence or building structures protected by antifouling paints (boats, dock pilings and farming systems). From the above, and considering the long life estimated for TBT, remaining for decades (Miloslavich et al., 2007), it is expected that the sediment will have a high concentration of this organotin compound, of ancient or recent origin.

Imposex proportion and degrees

The occurrence of pseudopenis and vas deferens in females of Thaisella chocolata from Caldera Bay is consistent with the characterization of the imposex syndrome described by Smith (1971). The proportion of imposex determined in the sample of this study is the maximum possible (I% = 100%); taking into account, 1) the number of samples analyzed (n = 90), 2) the random nature of the sample, and 3) a collection after this study of 60 females with I% = 100% was obtained at 10 km from the original site collection, it is expected that imposex is a widespread phenomenon in the population of T. chocolata in this location.

Most imposex scales used in this study (Gibbs et al., 1987; Stroben et al., 1992; Fernandez et al., 2002; Rodriguez et al., 2008) coincide in extreme masculinization of T. chocolata. However, the scale of Stroben et al. (1992) is the most integrated in representing in detail macroscopically and histologically all the symptoms of imposex, especially in the area of the vagina; these characteristics were observable in the ninety females of T. chocolata from Caldera Bay. The scale of Barreiro et al. (2001) is an exception, since it classified the degree of convolution of the oviduct in females affected by imposex, and apparently reflects its gradual transformation toward a seminal vesicle (Oehlmann et al., 1991). This phenomenon has been described only in Nassarius reticulatus (Linnaeus, 1758) (Barreiro et al., 2001; Rodriguez et al., 2008) and Nucella lapillus (Linnaeus, 1758) (Oehlmann et al., 1991). Despite the occurrence of imposex advanced degrees in T. chocolata, convolution of the oviduct was not recorded, suggesting specific species sensitivity on this part of the system.

The indices of the Vas Deferens Stages Index (VDSI), Relative Penis Length Index (RPLI) and Relative Penis Size Index (RPSI) were adequate to represent the severity of imposex in T. chocolata, since high values reflected proportionally a greater development of pseudopenis, vas deferens and occlusion of the vulva compared to those reported for other gastropods with similar values in these indexes, VDSI = 4.0 (Fernandez et al., 2002), RPLI = >50 points (Lahbib et al., 2008; Castro & Fillmann, 2012) and RPSI = >20 points (Spence et al., 1990). We recommended the VDSI index for T. chocolata; this index provides a realistic measure of the virilization and reproductive potential of the females of gastropods affected, as well as also its value represents a estimating the concentrations of TBT in the environment (Fioroni et al., 1991; Schulte-Oehlmann et al., 1997), and would not be affected by the sigmoid shape and size of the penis (Vasconcelos et al., 2011).

The occurrence of imposex has been reported in seven other species of gastropods in Chile (Gooding et al., 1999; Huaquin et al., 2004; Panes, 2004; Collado et al., 2010; Vasquez, 2015; Batista et al., 2016). Gooding et al. (1999) used the Stroben et al. (1992) scale to establish the degree of imposex in Chorus giganteus (Lesson, 1830), Nucella crassilabrum (Lamarck, 1816) [=Acanthina monodon (Pallas, 1774)] and Xanthochorus cassidiformis (Blainville, 1832). The authors determined degrees <4, that is, different degrees of development of pseudopenis and vas deferens that would not prevent normal reproduction. By contrast, the degree of masculinization determined in the present study with the same scale is associated with total sterility of T. chocolata from Caldera Bay.

Castro & Fillmann (2012) determined, in several localities from Peru, that T. chocolata suffered degrees of imposex of 1-5 on the scale of Gibbs et al. (1987). The authors found a positive relationship between the concentration of organotin compounds in tissues (23.5 -662 ng Sn/g-1 dry weight) and the degree of imposex. According to data reported by Castro & Fillmann (2012), one would expect that the concentration of TBT in specimens of T. chocolata from Caldera will exceed 662 ng Sn/dry weight. This will be confirmed by analyzing the concentrations of TBT in sediments and tissues of this species (work in progress).


Thaisella chocolata is the eighth species described with imposex in Chile and the first reported for the northern area. The degree of imposex determined in Caldera Bay corresponds to the most advanced stage and is associated with the total sterility of this species in this locality.

The scale of Stroben et al. (1992) is the most appropriate to characterize imposex, describing the most observable and conspicuous alterations of this syndrome in the 90 females of T. chocolata analyzed. VDSI is suggested as the best imposex index since it would not be affected by the shape and/or size of the male penis.

Considering the abundance and wide geographic distribution of T. chocolata, we believe it would be advisable to use this species as a potential bioindicator of pollution by organotin compounds on the coast from northern Chile. Currently, it is working on determining the concentration of butyltin compounds in sediments and tissues of T. chocolata from sites with different grades of antropic activity.

DOI: 10.3856/vol44-issue4-fulltext-18

Received: 15 November 2015; Accepted: 29 July 2016


We thank Dra. Karin Lohrmann for her supports with histologycal techniques, to Mr. Helmo Perez Jr. and Mr. Jose Parra for collecting specimens, as well as the evaluators for their corrections and suggestions.


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Yasna Mattos (1) & Maria Soledad Romero (1)

(1) Departamento de Biologia Marina, Facultad de Ciencias del Mar Universidad Catolica del Norte Coquimbo, Chile

Corresponding author: Yasna Mattos (

Corresponding editor: Cristian Aldea

Caption: Figure 1. Thaisella chocolata. Pseudopenis and penis: a-c) Macroscopic view of the pseudopenis. a) Location of the pseudopenis, behind the right tentacle. In the anterior part of the pseudopenis is located a filiform extension, b) occurrence of two pseudopenis, c) dense structure (arrowhead) and pseudopenis tissue fusion. Scale bar: 1 cm, dg: digestive gland, f: filiform, me: mantle edge, o: ovary, pp: pseudopenis, r: rectum, rt: right tentacle, tf: tissue fusion.

Caption: Figure 2. Trasnverse histological sections of the pseudopenis duct and penis duct of Thaisella chocolata. a) Narrow lumen (arrow) of the pseudopenis duct and surrounded by a thick circular musculature in female (scale bar = 400 [micro]m), b) Lumen (arrow) of the penis duct surrounded by a circular muscle in male. (scale bar = 300 pm). m: muscle.

Caption: Figure 3. Lineal correlation of the shell length (mm) and pseudopenis/penis length (mm) of females and males of Thaisella chocolata from Caldera Bay.

Caption: Figure 4. Vulva of Thaisella chocolata female, a) Macroscopic view of vulva occluded by the vas deferens (scale bar = 1 cm), b) transverse histological section of prostatic glands (arrows) on the periphery of the vulva musculature (scale bar = 200 [micro]m). cg: capsule gland, v: vulva, vd: vas deferens, vm: vulva musculature.

Caption: Figure 5. Capsule gland from female Thaisella chocolata. a) External view of the gland. Note the nodular structures, b) gland with aborted ovicapsule mass (arrow). Inset: external view of aborted ovicapsule mass, a-b (scale bar = 1 cm). c-f) transverse histological sections of capsule gland, c) modified cylindrical epithelium of the gonoduct (scale bar = 80 [micro]m), d) glandular tissue with acellular areas and low dye affinity (arrows) (scale bar = 20 [micro]m), e) detail of pyknotic nuclei (arrows) (scale bar = 5 [micro]m), f) prostatic glands on the periphery of capsule gland (scale bar = 70 [micro]m). cg: capsule gland, cyl: cylindrical, cub: cubic, n: nodular, r: rectum, pg: prostatic gland.

Caption: Figure 6. Ingestive gland of female Thaisella chocolata transverse histological section: Saccules of ingestive gland. It highlighted on the periphery of the gland, the occurrence of acini of prostatic gland (arrows). Scale bar = 200 [micro]m, sc: saccules.

Caption: Figure 7. Albumen gland from a female Thaisella chocolata', transverse histological sections a) modified cylindrical epithelium of gonoduct (scale bar = 70 [micro]m), b) gonoduct epithelium with lack of basal lamina (scale bar = 20 [micro]m), c) diffuse demarcation (arrows) between albumen and capsule glands, d) acini of prostatic gland on the periphery of albumen gland. c-d scale bar = 200 [micro]m, ag, albumen gland, cg, capsule gland, cyl, cylindrical, ps, pseudostratified.
Table 1. Percent (%) and number (n) of imposex degree in
90 females of Thaisella chocolata on the scales of Gibbs et
al. (1987), Stroben et al. (1992), Barreiro et al. (2001),
Fernandez et al. (2002) and Rodriguez et al. (2008).

Scales         Characterization of the      Degree     %    n
               vas deferens degree

Gibbs et       Complete development            4      34    31
  al. (1987)     of vas deferens.
               Vagina blocked by               5      44    40
                 vas deferens.
               Aborted ovicapsules in          6      22    19
                 the capsule gland.
Stroben et     Pseudopenis with penis          4      40    36
  al. (1992)     duct and vas deferens
                 continuous. Also
                 includes the occurrence
                 of two pseudopenises
                 in females.
               Vagina reduced or absent.      5a      10    9
                 Prostate gland
                 of variable
                 length arises in
                 the mantle cavity.
               Vagina occluded by the         5b      34    30
                 vas deferens, often
                 forming nodules.
               Vagina reduced or absent.      6a       4    4
                 Occurrence of aborted
                 ovicapsules in the
                 capsule gland.
               Vagina occluded by the         6b      12    11
                 vas deferens. Occurrence
                 of aborted ovicapsules
                 in the capsule gland.
Barreiro et    Rectilinear, transparent        0      100   90
  al. (2001)     and narrow oviduct.
Fernandez et   Pseudopenis (>1 mm) and/or      3      10    9
  al. (2002)     vas deferens incomplete.
               Vas deferens continued.         4      30    27
               Vagina blocked by               5      44    40
                 the vas deferens.
               Aborted ovicapsules in          6      16    14
                 the capsule gland.
Rodriguez et   Hard aborted ovicapsules        4      16    14
  al. (2008)     impossible to break.
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Title Annotation:Research Article
Author:Mattos, Yasna; Romero, Maria Soledad
Publication:Latin American Journal of Aquatic Research
Article Type:Ensayo
Date:Sep 1, 2016
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