Indian Journal of Marine Sciences Vol. 31(3), September 2002, pp. 243-245

Short Communication

Imposex in muricid gastropod Thais biserialis (: : ) from Tuticorin harbour, southeast coast of India

M. Santhana Ramasamy & A. Murugan* Suganthi Devadason Marine Research Institute, 44-Beach Road, Tuticorin- 628 001, Tamil Nadu, India [ *E-mail: a_ _ [email protected] ] Received 21 November 2001, revised 15 May 2002

Imposex has been reported in the muricid gastropod Thais biserialis from inside the Tuticorin port. The sex ratio de- parted from 1:1 and the males were dominant. The frequency of imposex in females was 35%. The Vas deferens sequence (VDS) index indicated the occurrence of initial imposex stages of 1a and 2a i.e. the development of penis and penis with closed duct. The Relative penis size (RPS) index values were less when compared to the reports elsewhere. The observation of imposex indicated the possible contamination of tributyltin (TBT), which could have leached out from antifouling paints of the ships using Tuticorin port.

[ Key words: tributyltin, TBT, imposex, gastropod, muricid, Tuticorin, Thais biserialis ]

Antifouling paints containing tributyltin (TBT) com- Tuticorin Port was declared as the 10th Indian Ma- pounds were introduced in 1960s and found wider use jor Port in 1974 and the traffic is increasing every from mid 1970s. TBT is used as the active biocide in year- 899 vessels in 1998-99 to 1236 vessels in 2000- marine antifouling paints and also used as paper, 2001. There is no dry dock facility at the Port. The wood and textile preservatives, plastic, especially possibility of TBT contamination through leaching PVC stabilizers and as slimicides for cooling towers1. from antifouling paints from ships is more in Tuti- The abnormal growth and reproductive failure in cul- corin Port area. Hence, the study has been taken up to tivated oyster, Crassostrea gigas in Arcachon Bay in assess the possible effect on gastropod Thais biseri- France was linked to the leaching of TBT from anti- alis (Blainville) (Mollusca:Neogastropoda: Murici- foulants on small boats2. It has been proved that TBT dae) distributed inside the port area. causes imposition of male sex characters in females of Sixty two of Thais biserialis were col- neogastropods and this is particularly well reported in lected from inside the port area of Tuticorin (lat. 8º muricid gastropods3. Imposex is known in 72 species 45′ N and long. 78º 13′ E). The collected specimens of gastropods belonging to 49 genera4. The develop- were transported in live condition to the laboratory, ment of male sex characters including penis and vas cleaned and maintained with aeration until further deferens in extreme cases, occludes the genital pore analysis. The animals were narcotized using 7% causing the female sterile and some times lead to MgCl and shell length was recorded to the nearest premature mortality due to build up of egg capsules in 2 0.1 mm. The shells were cracked by light taps with a the capsule gland. hammer and the soft parts removed. The sex was de- Imposex is prevalent in places close to ports, ship- termined by the presence of prostate gland in males yards, marinas and around mariculture facilities where and the capsule gland, albumen gland in females. The organotin compounds are used in antifouling paints5. length of the penis in both males and females (with Among the muricid gastropods, species mainly be- imposex) were measured using occulometer under the longing to the Thais have been used as indica- binocular microscope. The imposex frequency was tors of TBT contamination in tropical waters6. TBT calculated as the proportion of females with imposex has been attributed to the local extinction of some compared with the total number of females sampled5. populations of dogwhelks, Nucella lapillus in South- The condition of the vas deferens in females was as- west England6. In India, imposex has been recorded in sessed using the vas deferens sequence (VDS) index8. Cronia konkanensis from Marmagoa harbour7. Relative penis size (RPS) index is expressed as7: 244 Indian J. Mar. Sci., Vol. 31, No. 3, September 2002

Table 1 ⎯ Imposex in Thais biserialis from Tuticorin port area

Number of Sex Shell Penis Imposex in RPS RPL VDS individuals length length females (%) (%) (%) (mm) (mm) (%) (mean ± SD) (mean ± SD) Whole sample

42 M 22 ± 2.6 2.8 ± 0.5 ⎯ ⎯ ⎯ ⎯ 20 F 23.3 ± 2.6 0.4 ± 0.1 35 0.3 14.3 0.7 Imposex stages in females Stage No. %

0 13 65 24.1 ± 2.7 ⎯ ⎯ ⎯ ⎯ ⎯ 1a 1 5 2.3 0.3 ⎯ 0.1 10.7 ⎯ 2a 6 30 23.2 ± 3.1 0.4 ± 0.1 ⎯ 0.3 14.3 ⎯

(Mean length of female penis) 3 i.e. development of penis and penis with closed duct. ×100 (Mean length of male penis) 3 The stage 2a is prevalent and occurred in 86% of the 7 females with imposex. It has been indicated that a Relative penis length (RPL) index is expressed as : population with an VDS index of above 4 has steril- Mean length of female penis ×100 ized females and thus have a reduced reproductive Mean length of male penis capacity9. However, in the present study VDS index In Thais biserialis distributed in Tuticorin port value of 0.7 was observed and is well within 4. No area, the average length of the male and female shells occlusion of genital pore or aborted capsules was no- was 22 mm and 23.3 mm. A marked deviation in the ticed during the present observation. male : female sex ratio was 2.1 : 1. Similar deviation The TBT based antifouling paints used in ships and in sex ratio with male dominance has been observed boats have affected the non-target organisms as well, in T. bitubercularis, T. clavigera and T. jubilaea from especially the molluscs. Among the muricid gastro- Singapore3. The frequency of imposex was 35% and it pods, species belonging to Thais sp. have been used is less when compared to the recorded range of 90 – as indicators of TBT contamination in tropical wa- 1 100% from Marmagoa harbour7 and in Phuket, Thai- ters . Whereas, Nucella lapillus is the commonly used land5. The mean penis length of the male was 2.8 mm indicator of TBT contamination in temperate zones 10 and that of female with imposex 0.4 mm. The correla- because of its abundance and sensitivity to TBT . But tion between male shell length and penis length the observation of imposex in Nucella lapillus from [0.0460 (P > 0.05)] and that of female shell length and the shore adjacent to a gull roost and near breeding penis length [−0.0468 (P > 0.05)] were not significant. colonies of seabirds in UK which has been attributed The RPS index value was 0.3% and RPL index was to the compounds from birds excretion has implica- 14.3% (Table 1). The RPS index did not exceed 25% tions on the use of imposex as an indicator of TBT 11 and is also less when compared to three Thais species level in the environment . However, TBT is consid- studied in Singapore3. RPL and RPS values increased ered as the most toxic compound ever deliberately 12 with increasing VDS stage. Similar increase in RPL introduced into the natural waters . TBT exhibits no and RPS index values corresponding to the VDS stage direct effect on the female genital system, but disturbs 13 has been observed for Cronia konkanensis from Goa7. the biosynthesis of steroid hormones . VDS index is considered as the more valid index for The present study showed the initial stages of pos- the biomonitoring of TBT pollution and VDS index sible TBT contamination. The unequal sex ratio and provides information on the reproductive capability of the observation of stages 1a and 2a of the VDS index the population8. The recognition of different stages in indicated the possible effect of TBT, which could vas deferens development provides a more sensitive have leached out from the antifouling paints of the method of categorising the intensity of expression of ships using the Tuticorin port. Though there is a pos- imposex9. The frequency of imposex assessed through sibility of inducement of imposex by other contami- VDS indicated the occurrence of stages8 1a and 2a, nants3, the widespread observation of imposex in

Short communication 245

muricid gastropods due to TBT indicate the possibil- England: Evidence for the effect of tributyltin from antifoul- ity of TBT contamination in the present study also. ing paints, J. Mar. Biol. Ass. U. K., 66 (1986) 611-640. Authors are thankful to DANIDA, Denmark for 7 Vishwa Kiran Y & Anil A C, Record of imposex in Cronia konkanensis (, Muricidae) from Indian waters, funding through the Tropical Marine Mollusc Pro- Mar. Env. Res., 48 (1999) 123-130. gramme. The data on port traffic provided by Tuti- 8 Oehlmann J, Stroben E & Fioroni P, The morphological ex- corin Port Trust is gratefully acknowledged. pression of imposex in Nucella lapillus (Linnaeus) (Gastro- poda: Muricidae), J. Moll. Stud., 57 (1991) 375-390. References 9 Gibbs P E, Bryan G W, Pascoe P L & Burt G R, The use of 1 Rexrode M, Ecotoxicology of tributyltin, in International the dog-whelk, Nucella lapillus as an indicator of tributyltin Organotin Symposium of the Oceans’87 conference proceed- (TBT) contamination,. J. Mar. Biol. Ass. U. K., 67 (1987) ings, vol. 4 (IEEE, New York) 1987. pp. 1443-1455. 507-523. 2 Alzieu C, Environmental problems caused by TBT in France: 10 Bryan G W, Gibbs P E, Burt G R & Hummerstone L G, The Assessment, regulations and prospects, Mar. Env. Res., 32 effects of tributyltin (TBT) accumulation on adult dog- (1991) 7-17. whelks, Nucella lapillus, J. Mar. Biol. Ass. U. K., 67 (1987) 3 Tan K S, Imposex in three species of Thais from Singapore, 525-544. with additional observation on T. clavigera (Kuster) from Ja- 11 Evans S M, Kerrigan E & Palmer N, Causes of imposex in pan, Mar. Pollut. Bull., 34 (1997) 577-581. the dogwhelk Nucella lapillus (L.) and its use as a biological 4 Fioroni P, Oehlmann J & Stroben E, The pseudohermaphro- indication of tributyltin contamination, Mar. Pollut. Bull., 40 ditism of prosobranchs: Morphological aspects, Zoologischer (2000) 212-219. Anzeiger., 226 (1991) 1-26. 12 Goldberg E D, TBT: An environmental dilemma, Environ- 5 Michael Bech, Increasing levels of tributyltin-induced im- posex in muricid gastropods of Phuket Island, Appl. Or- ment, 28 (1986) 17-44. ganometal. Chem., 13 (1999) 799-804. 13 Oehlmann J, Stroben E & Fioroni P, New facts about tribu- 6 Bryan G W, Gibbs P E, Hummerstone L G & Burt G R, The tyltin-induced imposex in Prosobranchs: General aspects, decline of the gastropod Nucella lapillus around south-west Malacological Review, Supplement 6 (1996) 149-156.