Indian Journal of Marine Sciences Vol. 31(4), December 2002, pp. 321-328

Imposex in rock whelks and Ocenebra (, , ) from Gujarat coast

A. Tewari, C. Raghunathan, H. V. Joshi & Yasmin Khambhaty Central Salt and Marine Chemicals Research Institute, Bhavnagar-364 002, Gujarat, India Revised 3 October 2001, revised 19 July 2002

Imposex in Thais bufo, T. rudolphi, T. tissoti and Ocenebra bombayana was observed from Saurashtra coast of Gujarat. The maximum percentage of imposex out of total sample size (44.80 and 46.55%) were observed at Porbandar in T. bufo and T. rudolphi respectively while T. tissoti and O. bombayana at Mahuva showed 10.29 and 9.72% of imposex respectively. The percentage conversion of potential females to imposex was minimum at Diu and maximum at Porbandar. The number of ships operated from Porbandar and Diu directly correlated with severity of CPFII and percentage of imposex at these places. The results indicate that severity of imposex in T. rudolphi could be utilized as a bioindicator of TBT contamination in the marine environment. The Relative Penis Size Index(RPSI) ranged from 3.24 at Veraval to 16.50 at Porbandar in T. bufo while in T. rudolphi it ranged from 44.26 at Okha and 55.96 at Veraval. It was 21.19 and 14.26 for T. tissoti and O. bombayana respectively. The results indicate that RPSI may not be a foolproof indicator of severity of imposex in these organisms. Therefore a new index has been developed which is termed as Conversion of Potential Females to Imposex Index (CPFII) to calculate the potential females of a given area of a population. It seems the causative agents in seawater is neither toxic nor growth inhibitory at all the places of study but it interferes with the reproductive mechanisms and morphogenesis in these four species. The imposex in these organisms and its relation to TBT concentration in the marine environment is discussed. [ Key words: Imposex, neogastropods, Thais, tributyltin ]

Imposex is the superimposition of male sex organs, prohibited from the year 2003 onwards10. Vessels penis and vas deferens on the female own genital must be free of these coatings10 altogether by 2008. system in gonochoristic gastropods1. It is also called These proposals are part of a stepwise approach by pseudohermaphroditism. In advance cases the imposex IMO, whereby all antifoulants which exhibit may bring out reproductive failure and consequential potentially harmful effects in the marine environment population decline1,2. The reproductive failure leads to will eventually be banned10. sterility in females and in extreme cases, the whole Imposex has been described in 118 species of neo- population vanishes from that area. The imposex is gastropods, belonging to 63 genera11. But, informa- reported to be caused by organotin compounds like tion on imposex in gastropods from Indian coastal tributyltin (TBT), triphenyltin3 etc. which are used as waters is not available. However, the effect of TBT on anti-fouling paints in ships, fishing nets and the toxicity of some bivalves under laboratory condi- mariculture cages4,5. The imposex occurs at levels of tions has been reported12. TBT contamination as low as parts per trillion, Muricid gastropods especially Chicoreus, Thais, however, it can be caused by agents other than TBT Murex etc. are commercially important as regular diet including parasitic trematode larvae6 and other and other products. Since it has got widespread eco- important pollutants such as copper compounds7 and nomic implications, the present study was taken to nonylphenol8. However the effect of copper on examine the severity of imposex on Gujarat coast, imposex has not been proved9. All ships including which is the second largest industrialized state of Indian ships use the antifouling paint containing TBT India. as there is no regulation as on date in India and several other countries to ban the use of TBT in Materials and Methods antifouling paints. International Maritime Organiza- The specimens of rock whelk Thais bufo (Lamarck) tion (IMO) is expected to endorse a recommendation and Thais rudolphi (Lamarck) were collected from from its Maritime Environmental Protection Committee Gujarat coastline--Okha (lat.22° 30′N, long.69° 03′E), that the application of TBT based coatings should be Dwarka (lat.21° 15′N, long. 68°41'E), Porbandar 322 Indian J. Mar. Sci., Vol. 31, No. 4, December 2002

(lat.21° 39′N, long. 69° 38′E), Mocha (lat.21° 20′N, long. 69° 53′E), Veraval (lat.20° 54′N, long. 69° 53′E) and Diu (lat.20° 43′N, long. 70° 47′E). Thais tissoti (Petit) and Ocenebra bombayana (Melvill) were collected from Mahuva (lat.21° 05′N, long. 71° 47′E) (Fig. 1). They were collected from the intertidal region of the rocky coasts during October and November 2000. Specimens of each species were randomly collected during low tide in considerable numbers for imposex studies. Soon after collection, the epiphytic flora and fauna on the surface of the shell were thoroughly removed and washed with clean seawater. The were preserved in ice cold Fig. 1 ⎯ Location of sampling sites condition and transported to laboratory where the morphometric measurements such as shell length and of Potential Female to Imposex Index (CPFII). The weight were measured by vernier caliper and analyti- formula for the index is : cal balance respectively. The morphometric meas- Number of imposex animals CPFII = ×100 urements were made with a view to identify the Number of females + Number of growth stage at which imposex occurs. The shell of imposex animals the rock whelks were cracked carefully and the soft The density of four species at all sampling stations tissues were gently removed for the determination of were also estimated from their natural habitat along sex and imposex. Only reproductively matured indi- 2 viduals were studied during the investigation. Sex was the intertidal belt by 0.5 m quadrate having 10 × 10 cm determined primarily by the presence of bright yellow sub quadrates. Data were collected at every 5 m inter- ovaries in the case of females and orange testes for val starting from 0.32 m at Okha and Dwarka, 0.21 m males and both of these are located ventrally in the at Porbandar and Mocha, 0.45 m at Veraval, 0.52 m at coiled section adjacent to the digestive gland on the Diu and Mahuva (taken as baseline) above the zero of posterior of the . In addition to that sex was the chart datum extending towards highest high tide also confirmed by the presence of capsule gland, mark. The density in terms of numerical abundance sperm ingesting gland and albumen gland on the ante- and biomass per unit area was determined. The stan- rior to the ovary for females and prostate gland for dard deviation and correlation coefficient were deter- males in the same position. Imposex was identified in mined by Microsoft Excel software. females by the formation of vas deferens and devel- The turbidity was determined by turbidity meter opment of penis behind the right cephalic tentacle. (Model HANNA HI 93703). The number of ships The length and width of the penis of males and im- operating from Okha (near Dwarka), Porbandar (near posex specimens were measured from its tip to junc- Mocha), Mul Dwarka (near Veraval and Diu) and Pi- tion with the wall to 0.1 mm using an eye piece pavav (near Mahuva) during different years were col- graticule mounted on a binocular stereozoom micro- lected from the concerned port authorities. scope. The penises were then excised at their bases and dried to constant weight at 60ºC and the dried Results tissue was weighed to the nearest 10 µg using an ana- The length, weight, percentage occurrence of lytical balance. The intensity of imposex development males, females and imposex and CPFII of T. bufo and in animals were calculated by Relative Penis Size In- T. rudolphi in different stations is presented in Table 1. dex(RPSI) using the following formula4; The maximum percentage of imposex out of total sample size(44.80 and 46.55 %), were observed at Mean length of imposex penis 3 Porbandar in T. bufo and T. rudolphi respectively RPSI = ×100 Mean length of male penis 3 (P < 0.01, r = 1 for both) (Fig. 2). However the mini- mum percentage in these organisms (11.90 and A new index has been developed to calculate the po- 13.76 % respectively) were observed at Diu (P < 0.01, tential females of a given area of population con- r = 1). The CPFII was minimum at Diu and maximum verted to imposex. This index is termed as Conversion at Porbandar. The least CPFII (22.22 and 25.86) in

Tewari et al.: Imposex in rock whelks 323

T. bufo (P < 0.05, r = 0.62) and T. rudolphi (P < 0.01, and CPFII in O. bombayana were 9.72 % and 16.07 r = 1) respectively were observed at Diu and highest respectively. The length and weight of O. bombayana (71.80 and 71.05 respectively) were recorded at were least in imposex animals and highest in males Porbandar. The number of ships operated from (P < 0.05, r = 0.62). Porbandar and Diu directly correlated with severity of The mean length, width and dry weight of penis in CPFII and percentage of imposex at these places normal and imposex animal as well as Relative Penis (Tables 1, 2). The weight and length of males, Size Index (RPSI) for T. bufo and T. rudolphi are pre- females and imposex of T. rudolphi were always sented in Table 4 and for T. tissoti and O. bombayana higher than T. bufo at all the stations studied (P < 0.01, in Table 5. The RPSI ranged from 3.24 at Veraval to r = 1). 16.50 at Porbandar in T. bufo (P < 0.05, r = 0.81) while Thais tissoti and Ocenebra bombayana were re- in T. rudolphi (P < 0.01, r = 1) it ranged from 44.96 at corded only from Mahuva where seawater is turbid Okha and 55.96 at Veraval. The mean length, width (turbidity 50.00 to 76.00FTU) and the growth of ben- and dry weight of penis in normal males and imposex thic marine algae is least, whereas T. bufo and of T. bufo and T. rudolphi were always least at Diu T. rudolphi were recorded from Okha, Dwarka, and highest at Porbandar (P < 0.01, r = 1). However, Porbandar, Mocha, Veraval and Diu. The seawater in the minimum dry weight of T. bufo was observed at these places had very low turbidity (turbidity 3.21 to Veraval and maximum at Okha in imposex penis. 6.45 FTU) and the growth of seaweeds was luxuriant. RPSI for T. tissoti was 21.19 while mean length,

The length, weight and percentage occurrence of male, female and imposex of T. tissoti is depicted in Table 3. The percentage of imposex out of total sam- ple size in T. tissoti was 10.29 % and CPFII was 17.07 (P < 0.05, r = 0.85 for both). The results indicate that T. rudolphi (P < 0.01, r = 1) was more sensitive and T. tissoti was least. However, the length and weight of T. tissoti at Mahuva were much less as compared to that of T. bufo and T. rudolphi at other six places (P < 0.05, r = 0.53 for both) (cf. Tables 1,3). The length, weight, occurrence of male, female and im- posex and CPFII of O. bombayana is shown in Table 3. The percentage of imposex out of total sample size, Fig. 2 ⎯ Imposex in T. bufo

Table 1 ⎯ Percentage of imposex, males and females of Thais bufo and Thais rudolphi and their morphometric measurements Station Sample Male Female Imposex CPFII size % of total Mean Mean % of total Mean Mean % of total Mean Mean population length weight population length weight population length weight (mm) (g) (mm) (g) (mm) (g) Thais bufo Dwarka 110 47.27 38.52 19.76 30.00 37.32 21.38 22.73 36.58 17.36 43.90 Porbandar 125 37.60 43.18 21.17 17.60 42.53 25.76 44.80 41.76 19.82 71.80 Mocha 120 44.17 42.56 20.79 31.66 41.50 23.39 24.17 40.50 16.23 43.28 Veraval 96 46.87 35.52 16.38 34.20 33.75 18.20 15.62 32.86 15.19 29.41 Diu 84 46.43 35.28 17.00 41.50 34.20 19.76 11.90 32.88 14.10 22.22 Thais rudolphi Okha 95 36.84 41.88 23.85 23.16 42.80 24.52 40.00 40.28 20.70 63.33 Dwarka 106 44.34 44.72 26.58 26.41 43.12 23.33 29.25 41.50 22.16 52.54 Porbandar 116 34.48 44.86 28.32 18.97 43.50 26.58 46.55 40.76 21.24 71.05 Mocha 88 43.18 43.38 21.74 22.73 45.72 25.95 34.09 46.34 25.75 60.00 Veraval 107 35.52 41.36 24.72 45.78 42.58 25.80 18.69 40.52 19.37 29.00 Diu 109 46.79 40.10 22.36 39.45 41.34 24.83 13.76 39.26 17.21 25.86

324 Indian J. Mar. Sci., Vol. 31, No. 4, December 2002

Table 2 ⎯ Number of ships handled by port nearer to study sites on Gujarat coast Year Number of commercial vessels operated Okha Porbandar MulDwarka Pipavav (near Dwarka) (near Mocha) (near Veraval and Diu) (near Mahuva) 1996-1997 91 117 44 13 1997-1998 105 123 61 33 1998-1999 62 72 44 − 1999-2000 96 113 40 − 2000-2001 73 95 63 −

− data not available

width and dry weight of penis both in normal and Table 3 ⎯ Percentage of imposex, males and females and their imposex animals were less when compared to T. bufo morphometric measurements of T. tissoti and O. bombayana at Mahuva and T. rudolphi (P < 0.01, r = 1). The RPSI of O. bombayana was 14.26. The mean length, width Parameters T. tissoti O. bombayana and dry weight of penis in normal and imposex ani- Mean length (mm) mals were less than T. bufo (P < 0.05, r = 0.78) and Male 20.10 28.30 T. rudolphi (P < 0.01, r = 1) but more than T. tissoti. Female 21.22 27.50 The individual animal density and biomass density Imposex 20.16 26.38 at different places in the intertidal belt for T. bufo, Mean weight (g) T. rudolphi, T. tissoti and O. bombayana are given in Tables 6 and 7. The individual animal density ranged Male 2.41 3.58 -2 Female 2.32 3.27 from 4 at Diu and Veraval to 72 n.m at Porbandar Imposex 1.97 3.09 and Mocha for T. bufo (P < 0.01, r = 1) while it ranged Sample size (no.) 68 72 from 4 at Diu to 60 n.m-2 at Porbandar for T. rudolphi Male (% in total 39.71 40.28 population) (P < 0.01, r = 1). In general, the minimum density was recorded at 25-30m above the baseline while the Female (% in total 50.00 50.00 population) maximum was at 10-15 m for all the places studied. Imposex (% in total 10.29 9.72 The biomass availability for T. bufo ranged from population) 83.48 at Diu and Veraval to 2574.48 g.m-2 at Dwarka CPFII 17.07 16.07 -2 (P > 0.05, r = 0.81) followed by 2187.36 g m at Porbandar while for T. rudolphi it varied from 72.92 Discussion -2 at Diu to 2079.60 g.m at Porbandar (P < 0.05, The present results indicate that widespread im- r = 0.74). In general the minimum biomass for T. bufo posex is present in species of Ocenebra and Thais on was recorded at 30 m while the maximum at 5-10 m Gujarat coast. High degree of imposex (44.80 and above the baseline. However, the minimum biomass 46.55 %) has been observed in T. bufo and T. rudolphi for T. rudolphi was observed at 25-30 m and maxi- respectively. Similarly a very high CPFII has also mum at 15 m above the baseline. Thais tissoti and been observed (71.80 and 71.05 respectively) in these Ocenebra bombayana showed reverse trend for nu- two species. The maximum percentage of imposex merical and biomass densities (P < 0.01, r = 1 for and maximum CPFII was at Porbandar and the mini- both). The minimum values for these two parameters mum at Diu/Mahuva. This data directly correlated were observed at baseline where the maximum were with the number of ships being operated from these at 35 m. The numerical density of T. tissoti and two ports (Table 2). This indicates that the TBT in the O. bombayana varied similar to T. rudolphi (P < 0.01, antifouling paints might be the causative agent for r = 1). However, their biomass density was much less imposex in the four species studied. The results indi- than T. bufo and T. rudolphi (P < 0.01, r = 1). The im- cate that situation in Gujarat coast is likely to be seri- posex was observed when the minimum length and ous as > 40 % of total population and > 70 % of poten- weight of T. bufo, (32.86 mm, 14.10 g) T. rudolphi tial females developed imposex which is the net loss (39.26 mm, 17.21g), T. tissoti (20.16mm, 1.97 g) and to the total population in this region. High percentage O. bombayana (26.38 mm, 3.09g). of imposex in neogastropods has also been reported

Tewari et al.: Imposex in rock whelks 325

from the different parts of the world10,13,14,15-18. In In many species of muricids imposex in females is these cases the percentage of imposex ranged from characterized by the presence of a pseudopenis whose 50-100 %. relative size with respect to the male penis is routinely Imposex is reported to be caused mainly by or- used for quantifing imposex severity20. In the present ganotin compounds especially by tributyltin which is study the maximum RPSI in T. bufo and T. rudolphi reported to be most effective11. Imposex in neogastro- has been observed at Porbandar and Veraval respec- pods has been reported as bioindicator of organotin tively. This does not clearly correlate with maximum compounds especially tributyltin in the marine envi- percentage of imposex in total sample size and maxi- ronment2,3,10,11,16,18,19. Therefore it could be expected mum conversion of females to imposex at Porbandar. that the concentration of organotin compounds espe- Probably RPSI may not be a foolproof indicator of cially TBT at the study sites must be in a considerable imposex in Indian conditions. It is reported that the concentration to induce imposex in Thais and Ocene- RPSI may not be entirely appropriate for all species of bra species. TBT is used as a constituent of anti- neogastropods since they have different penis fouling paints used for ships, fishing nets and maricul- shapes17,19-21. The RPSI has inherent difficulty in ture cages4,5. Since the present study sites are nearer measuring the length of the penis and change in penis to the ports where shipping activities are very com- size depending upon the environmental conditions23. mon (Table 2), therefore TBT might be the causative In addition to this Vas Deferens Size Index (VDSI)4,22 agent of imposex in India also. However, this needs has so far been unsuccessful for species affected by further study to confirm this observation. It may be imposex. This was the case for T. clavigera and noted that TBT at a concentration as low as parts per T. bronni in Japan19, Dicanthais orbita and Lepsiella trillion in seawater induces imposex in neogastro- vinosa in Australia7,16 and T. gradata and Chicoreus pods11. The tissues of imposex samples of T. clavig- capucinus in Singapore24. The CPFII gives an impact era and T. bronni have been reported to contain 10-20 of environment on the total potential female population ng g-1 of TBT19. Therefore it is essential to determine in relation to imposex animals of that area. Therefore it the concentration of TBT and other organotin com- is more reliable than RPSI and VDSI as these two indi- pounds in seawater, sediment and marine organisms ces are based on individual organelle which change of India. Since quite a number of marine organisms their shape and size depending upon environmental are edible, therefore, it may have an effect on human conditions like the tidal level at which the animal health. grows, pollution status of the environment etc.

Table 4 ⎯ Morphometric characteristics and Relative Penis Size Index(RPSI) of penis of males and imposex of Thais bufo and Thais rudolphi Station Male Imposex RPSI Mean length Mean width Mean dry wt. Mean length Mean width Mean dry wt. (mm) (mm) (mg) (mm) (mm) (mg) Thais bufo Okha 12.16 2.32 10.22 6.10 1.50 4.50 12.62 Dwarka 11.76 2.50 9.11 5.20 1.47 3.12 8.65 Porbandar 12.31 3.00 10.75 6.75 1.52 4.05 16.50 Mocha 11.16 2.16 9.25 4.50 1.20 2.20 6.55 Veraval 10.38 2.00 8.31 3.31 1.00 1.02 3.24 Diu 9.30 1.35 7.13 3.30 1.00 1.56 4.46 Thais rudolphi Okha 13.12 3.05 12.12 10.12 2.85 7.91 44.96 Dwarka 14.06 3.50 13.00 11.33 3.00 8.30 52.33 Porbandar 14.67 3.81 13.10 12.00 3.10 9.68 54.73 Mocha 12.63 2.56 11.40 10.33 2.00 7.05 54.71 Veraval 11.31 2.12 9.60 9.32 1.89 6.13 55.96 Diu 10.56 2.00 8.92 8.31 1.65 5.99 48.73

326 Indian J. Mar. Sci., Vol. 31, No. 4, December 2002

Thais rudolphi from different parts of Gujarat coast an exogenous substance that causes adverse health has shown very high percentage of imposex in total effects in an intact organism, or its progeny, secon- population, RPSI as well as CPFII (P < 0.01, r = 1 for dary to changes in endocrine function. In fact TBT all parameters). It seems that this species is very sen- induced imposex is the only known case of endocrine sitive to environmental conditions especially TBT disruption to occur at the population level26. Sex dif- which induce imposex. Therefore this organism may ferentiation in molluscs is a highly plastic process, be used as a bioindicator for TBT contamination un- which is under neuroendocrine control. There is evi- der Indian conditions. However, this aspects needs dence that TBT interferes with it by stimulating the further study. release of a morphogenetic factor by the pedal gland The minimum individual organism and biomass Table 5 ⎯ Relative Penis Size Index ( RPSI) of T. tissoti and densities were observed at Diu while maximum den- O. bombayana at Mahuva sity of these two parameters were observed at Parameters T. tissoti O. bombayana Porbandar/Dwarka. These results coincide with low percentage of imposex organisms at Diu and very Male high percentage at Porbandar. This indicates that the Mean penis length (mm) 5.2 6.7 concentration of causative agent in seawater is neither Mean penis width (mm) 2.0 2.10 toxic nor growth inhibitory to these organisms but it Mean penis dry weight (mg) 3.21 4.00 interferes with reproductive mechanisms and morpho- Imposex genesis resulting in increase of imposex leading to ultimate reduction of population. The imposex re- Mean penis length (mm) 3.1 3.5 sponse to neogastropods has shown that TBT is an Mean penis width (mm) 1.0 1.2 endocrine disrupter according to a definition produced Mean penis dry weight (mg) 2.98 3.15 by European Commission25: an endocrine disrupter is RPSI 21.19 14.26

Table 6 ⎯ Density of Thais bufo and T.rudolphi at different stations Distance Okha Dwarka Porbandar Mocha Veraval Diu from low Density Biomass Density Biomass Density Biomass Density Biomass Density Biomass Density Biomass tide to high- (no m-2) Fresh wt. (no m-2) Fresh wt. (no m-2) Fresh wt. (no m-2) Fresh wt. (no m-2) Fresh wt. (no m-2) Fresh wt. est high tide (g m-2) (g m-2) (g m-2) (g m-2) (g m-2) (g m-2) mark (m) Thais bufo 0 32 792.96 36 812.6 40 1410.8 44 1015.08 12 242.52 8 134.32 5 48 1396.80 44 1461.24 60 1709.4 64 1844.48 28 608.16 32 667.84 10 64 2099.20 52 1522.04 72 2187.36 72 1576.08 32 585.60 32 585.60 15 56 1270.08 68 2574.48 60 1576.20 56 1179.36 24 402.96 28 467.60 20 44 1324.84 60 1395.60 52 1173.12 48 1042.56 16 330.72 12 245.04 25 28 822.36 32 727.04 40 1328.40 36 828.72 12 245.04 4 83.48 30 20 440.20 16 432.48 28 819.56 24 568.08 4 83.48 − − Thais rudolphi 0 20 474.0 24 897.60 32 792.96 28 665.84 12 170.76 16 311.36 5 36 934.2 36 1487.5240 1164.00 32 832.36 20 344.20 16 259.36 10 40 878.0 52 1281.80 52 1554.80 44 1488.08 24 334.56 20 403.40 15 52 1716.0 44 1108.36 60 2079.60 52 1655.68 32 973.12 28 520.24 20 32 850.56 36 868.68 48 1574.40 48 1392.48 20 475.60 12 306.96 25 20 584.20 32 873.28 40 2154.80 32 817.60 16 383.04 4 72.92 30 12 254.16 12 300.24 28 920.08 28 622.16 12 351.36 − − −not available

Tewari et al.: Imposex in rock whelks 327

Table 7 ⎯ Density of T. tissoti and O. bombayana at Mahuva 6 Curtis L A, A decade-long perspective on a bioindicator of pollution: imposex in Ilyanassa absoleta on Cape Henlopen, Distance from T. tissoti O. bombayana Delaware Bay, Mar Environ Res, 38 (1994), 291-302. low tide to Density Biomass Density Biomass 7 Nias D J, McKillup S C & Edyvane K S, Imposex in Lep- −2 -2 highest high (no. m ) fresh wt. (no. m ) fresh wt. siella vinosa from Southern Australia, Mar Pollut Bull, -2 −2 tide (g m ) (g m ) 26 (1993) 380-384. mark (m) 8 Evans S M, Birchenough A C & Brancato M S, The TBT 0 4 9.72 4 11.68 Ban: Out of the frying pan into the fire?, Mar Poll Bull, 40 (2000) 204-211. 5 4 9.64 8 22.40 9 Claisse D & Alzieu, C, Copper contamination as a result of 10 12 28.56 20 62.00 anti-fouling paint regulations?, Mar Pollut Bull, 26 (1993) 15 20 55.60 28 89.60 395-397. 20 28 61.04 36 113.40 10 Evans S M, Kerrigan E & Palmer N, Causes of imposex in 25 32 79.36 40 126.80 the dogwhelk Nucella lapillus (L.) and its use as a biological indicator of tributyltin contamination, Mar Pollut Bull,, 30 48 131.52 52 170.04 40 (2000) 212-219. 35 56 157.36 64 229.12 11 Reitsema T J & Spickett J T, Imposex in Morula granulata 40 36 83.16 40 124.00 as bioindicator of tributyltin(TBT) contamination in the 45 28 59.36 32 112.00 Dampier Archipelago, Western Australia, Mar Pollut Bull, 50 12 23.76 12 38.40 39 (1999)280-284. 12 Karande A A, Ganti S S & Udhayakumar M, Toxicity of in female O. erinacea27. It could be concluded that tributyltin to some bivalves, Indian J Mar Sci, 22 (1993) 153-154. TBT contaminates from the paints severely increase 13 Terlizzi A, Geraci S & Minganti V, Tributyltin(TBT) pollu- the imposex in some of the species of neogastropods, tion in the coastal waters of Italy as indicated by imposex in consequently reducing the female population in that Hexplex trunculatus (, Muricidae), Mar Pollut area. This may lead to extension of these species in Bull, 36 (1998)749-752. the area where TBT contamination is severe. 14 Axiak V, Vella A J, Micallef D, Chircop P & Mintoff B, Im- posex in Hexaplex trunculus (Gastropdoa, Muricidae): first results from biomonitoring of tributyltin contamination in the Acknowledgement Mediterranean, Mar Biol, 121 (1995) 685-691. The authors are grateful to Dr. P.K. Ghosh, Director 15 Santos M M, Vieira, N & Santos A M, Imposex in the dog- for encouragement. The financial support provided by whelk Nucella lapillus(L.) along the Portuguese coast, Mar Pollut Bull 40 (2000) 643-646. Council of Scientific and Industrial Research, Gov- 16 Foale S, An evaluation of the potential of gastropod imposex ernment of India is gratefully acknowledged. Authors as a bioindicator of tributyltin pollution in Port Phillip Bay, are thankful to port authorities for providing shipping Victoria, Mar Pollut Bull, 26 (1993) 546-552. data. Sincere thanks are also due to Mr. B.R. Mehta 17 Wilson S P, Ahsanullah M & Thompson G B, Imposex in for his assistance during field study. neogastropods: an indicator of tributyltin contamination in eastern Australia, Mar Pollut Bull, 26 (1993) 44-48. 18 Evans S M, Evans P M & Leksono T, Widespread recovery References of dogwhelks, Nucella lapillus (L.), from tributyltin con- 1 Bryan G W, Gibbs P E, Burt G R & Hummerstone L G, The tamination in the North Sea and Clyde Sea, Mar Pollut Bull, decline of the gastropod Nucella lapillus around southwest 32 (1996) 263-269. England: Evidence for the effects of tributyltin form anti- 19 Horiguchi T, Shiraishi H, Shimizu M & Morita M, Imposex fouling paints, J Mar Biol Ass UK, 66 (1986) 611-640. and organotin compounds in Thais clavigera and T. bronni in 2 Gibbs P E & Bryan G W, Reproductive failure in populations Japan, J Mar Biol Assoc U K, 74 (1994) 651-669. of the dog-whelk Nucella lapillus, caused by imposex in- 20 Gibbs P E & Bryan G W, TBT-induced imposex in neogas- duced by tributyltin from antifouling paints, J Mar Biol Ass tropods snails: masculinization to mass extinction, in Case UK , 66 (1986)767-777. study of an environmental contaminant, edited by S.J. de 3 Horiguchi T, Shiraishi H, Shimizu M, Yamazaki S & Morita Mora (Cambridge University Press, Cambridge) 1996, M, Imposex in Japanese gastropods (Neogastropoda and pp. 212-236. Mesogastropoda): Effects of tributyltin and triphenyltin from 21 Stewart C, de Mora S J, Jones M R L & Miller M C, Im- antifouling paints, Mar Pollut Bull, 31 (1995)402-405. posex in New Zealand neogastropods, Mar Pollut Bull, 4 Gibbs P E, Bryan G W, Pascoe P L & Burt G R, The use of 24 (1992) 204-209. dog-whelk Nucella lapillus, an indicator of tributyltin(TBT) 22 Oehlmann J, Stroben E & Fioroni P, The morphological ex- contamination, J Mar Biol Ass UK , 67 (1987) 507-523. pression of imposex in Nucella lapillus (Lin- 5 Bryan G W, Gibbs P E & Burt G R, A comparison of the ef- naeus).(Gastropoda: Muricidae), J Mollus Stud, 57 (1991), fectiveness of tri-n-butyltin chloride and five other organotin 375-390. compounds in promoting the development of imposex in the 23 Bech M, Sensitivity of different muricid gastropods to tribu- dogwhelk, Nucella lapillus, J Mar Biol Ass UK, 66 (1988) tyltin contamination Phuket Mar Biol Cent Spec Publ , 611-640. 19 (1999) 151-156.

328 Indian J. Mar. Sci., Vol. 31, No. 4, December 2002

24 Tan K S, Imposex in Thais gradata and Chicoreus capucinus 26 Harrison P T C, Holmes P & Humfrey C D N, Reproductive (Mollusca, Neogastropoda, Muricidae) from the straits of Ja- health in humans and wildlife: are adverse trends associated hor: A case study using penis length, area and weight as meas- with environmental chemical exposure? Sci and Tot Environ, ures of imposex severity, Mar Pollut Bull, 39 (1999) 295-303. 205 (1997) 97-106. 25 EC, European workshop on the impact of endocrine disrupt- 27 Feral C & Lee Gall S, in Molluscan Neuroendocrinology, ed- ers on human health and wildlife, (European Commission, ited by Lever J. and Boer, H.H. (North-Holland, Amsterdam) Brussels) 1997. 1983, pp. 173-175. 50 (1996) 290-317.