Persistence of Tributyltin-Induced Imposex in Dogwhelks ( ) and Intersex in Periwinkles ( ) in Atlantic Canada

Transcription

1 Wter Qul. Res. J. Cnd, 2007 Volume 42, No. 2, Copyright 2007, CAWQ Persistene of Tributyltin-Indued Imposex in Dogwhelks ( ) nd Intersex in Periwinkles ( ) in Atlnti Cnd 1,3 1,2 Cmille Cory nd Shnnon M. Brd * Littorin littore Nuell lpillus Key words Nuell lpillus Littorin littore Introdution tretment is lking (Fent 1996). Hrmful effets of TBT on quti biot were first noted over qurter entury go in Arhon By, Western Frne (Alzieu et l. 1980). TBT exposure nd umultion were linked to oyster shell mlformtion, poor sptfll, nd ner ollpse of the lol oyster frming industry (Alzieu et l. 1980). TBT ontmintion hs sine been orrelted with vriety of detrimentl effets in quti nimls inluding endorine disruption in gstropods (Mtthiessen nd Gibbs 1998), impired immune funtion in Mytilus mussels (St-Jen et l. 2002; St-Jen et l. 2002b), nd immunotoxi nd genotoxi effets on fish nd other quti speies (Ptriolo et l. 2001; Tino et l. 2001). TBT hs lso been noted for its toxi effets in humns, inluding impirment of nturl killer ell funtion (Thoms et l. 2004). In TBT ontminted res, TBT hs been mesured in every quti orgnism smpled, from lower trophi level phytoplnkton nd snils to higher trophi level fish, sebirds, se otters, dolphins, whles, nd even humns (Knnn nd Flndysz 1997; Knnn et l. 1998; Tnbe et l. 1998).

2 Cory nd Brd Lepsiell vinos

3 Persistene of Imposex nd Intersex in Atlnti Cnd The purpose of the present study ws to determine the urrent inidene nd severity of both imposex in N. lpillus nd intersex in L. littore t sites within nd round Hlifx Hrbour. Current imposex nd intersex mesurements were ompred to those mde in 1995 (Prouse nd Ellis 1997) nd 1996 (Covert 1997) in order to ssess hnges tht my hve ourred due to the 1989 legisltive bn on TBT-use on vessels under 25 m in length, nd the 1999 bn preventing new ots of TBT ontining pint from being pplied on vessels of ll lengths ommening 1 Jnury The two indies of imposex (reltive penis size [RPS] nd the vs deferens sequene [VDS]) re strongly orrelted with onentrtions of tin s TBT in mbient sewter nd N. lpillus tissues (Gibbs et l. 1987; Glnte-Oliveir et l. 2006), nd were used to estblish grdients of TBT ontmintion in this study. In res where N. lpillus were bsent, intersex index (ISI) in L. littore ws used s mesure of TBT ontmintion (Buer et l. 1995; Oehlmnn et l. 1998). Study Are Mterils nd Methods Mesurements 3 3 Up to 42 dult L. littore were olleted from sites where N. lpillus were bsent (Admirl's Cove [n = 31], Birh Cove [n = 32], Drtmouth Cove [n = 42] nd Dingle [n = 38]) or not bundnt enough to smple (Herring Cove [n = 40] nd Long Cove Pond [n = 40]) while 20 to 40 dult L. littore were olleted from sites where N. lpillus were present nd bundnt enough to smple (BIO [n = 29], Continer Pier [n = 30], Ferguson's Cove [n = 20] nd Pt. Plesnt [n = 37]) (Tble 2). Speimens were nesthetized for two hours before exmintion in 7% (weight per volume) mgnesium hloride solution (in distilled wter). Shell height ws mesured to the nerest 0.1 mm nd weight in shell ws mesured to the nerest 0.01 g. The shell ws then rked open with mllet nd soft tissues were seprted from the shell remins to mesure weigh out of shell (g).the ISI, or verge intersex stge in popultion (totl number of intersex stges in smple per number of nlyzed femles), ws determined for eh site bsed on riteri estblished by Buer et l. (1995). Speimens exhibiting prsiti infetion were exluded from nlysis beuse prsitism n use onfounding modifition of the genitl system (Buer et l. 1995).The mle to femle rtio ws lso reorded. Sttistil Anlysis Fig. 1. Lotion of smpling sites in nd round Hlifx Hrbour, Nov Soti, Cnd for the 2006 dogwhelk (Nuell lpillus) imposex survey. Sites smpled in 1995 (Prouse nd Ellis 1997) s well re indited by irle. Sttistil nlyses were onduted using the omputer nlytil pkge SPSS For N. lpillus, orreltion mtrix using Person orreltion oeffiients ws reted to exmine orreltions between snil size (shell length [mm], weight in shell [g], weight out of shell [g], weight of shell [g]) nd penis length (mm) in both femle nd mle speimens t eh site. Liner regression

4 Cory nd Brd TABLE 1. b d d FPL, verge femle penis length; RPSI, Reltive femle to mle Penis Size Index (= FPL /Averge Mle Penis Length x 100); VDSI, vs deferens sequene index; M/F rtio, rtio of mles to femles. Imposex Frequeny = perentge of imposexed femles in popultion of dogwhelks. Suitble hbitt nd diet for ws found t these sites. Three were observed t the Herring Cove site in the spring, but none were found on the dte of smpling. Five were b d observed t the Long Cove Pond site in the spring, nd only one ws found on the dte of smpling. It is unler whether imposex is responsible for this lk of, or just nturl vrition in popultion numbers. It is possible tht imposex is responsible for the low number of t the Herring Cove site due to orresponding high rte of intersex in periwinkles surveyed there, but unlikely tht imposex is responsible for the low number of t the Long Cove Pond site due orresponding zero rte of intersex in periwinkles surveyed there.

5 Persistene of Imposex nd Intersex in Atlnti Cnd Littorin littore Site Dte of survey (dy/mo/yr) No. of Speimens Femle Mle Averge shell height (mm) ± SD Intersex frequeny (%) ISI b M/F rtio b Intersex frequeny = perentge of femle L. littore ffeted by intersex in popultion. ISI, intersex index; M/ F rtio, rtio of mles to femles. nlysis ws lso performed to test for orreltions between mle to femle rtios nd mesurements of imposex (RPSI, VDSI, nd imposex frequeny) t eh site. For L. littore, orreltion mtrix using Person orreltion oeffiients ws reted to exmine orreltions between femle snil size (shell height [mm], weight in shell [g], weight out of shell, weight of shell [g]) nd intersex stge. Liner regression nlysis ws lso performed to test for orreltions between mle to femle rtio nd intersex mesurements (ISI nd intersex frequeny) t eh site. Imposex Results b ' Fig. 2. Comprison of imposex frequeny in dogwhelks ( Nuell lpillus) surveyed t sites in Hlifx Hrbour, Nov Soti, Cnd in 1995 (Prouse nd Ellis 1997) nd 2006 (this work). Suitble hbitt nd diet for N. lpillus were found t these sites.

6 Cory nd Brd b Fig. 3. Comprison of RPSI in dogwhelks ( Nuell lpillus) surveyed t sites in Hlifx Hrbour in 1995 (Prouse nd Ellis 1997) nd 2006 (this work). Suitble hbitt nd diet for N. lpillus ws found t these sites. ' Intersex Fig. 4. Lotion of smpling sites in Hlifx Regionl Muniiplity, Nov Soti, Cnd for the 2006 periwinkle ( Littorin littore) intersex survey. Sites smpled in 1996 (Covert 1997) s well s 2006 (this work) re indited by irle. nd Dingle sites re loted in res where bundnt reretionl boting tkes ple. Despite urrent TBT bns, lk of enforement inreses the likelihood tht TBT ntifouling pint my be being used illeglly on these smller vessels. The Admirl's Cove site nd Birh Cove site re loted in the Bedford Bsin, bsin with entrl depression of up to 70 m deep. Fine-grined, orgni-rih sediments re deposited in ll of the deep wter res of Bedford Bsin (Bukley nd Winters 1992; Bukley et l. 1995). TBT hs high binding pity to finer prtiulte mtter like tht deposited in the Bedford Bsin, nd n persist for longer time periods nd t higher levels under suh onditions (Btley 1996). Sediment smples tken in 2002 ner the Birh Cove site showed deepwter sediments in the Bedford Bsin to ontin 56.9 ng of TBT- Sn per g (dry weight [d.w.]), whih is higher TBT level 6 b Three sites (BIO, Drtmouth Cove, nd Continer Pier) (Fig. 4) overlpped with sites tht were surveyed for L. littore intersex in 1996 (Covert 1997). ISI mesurements hve not hnged signifintly t ny of these sites in the lst dede: from 0.44 to 0.41 t the BIO site, from 0.76 to 0.67 t the Continer Pier site nd from 2.06 to 2.10 t the Drtmouth Cove site (Fig. 5). Disussion In 2006, the four surveyed sites lking N. lpillus within Hlifx Hrbour were loted within the inner hrbour in lose proximity to mrins, shipyrds, nd doking filities for lrge vessels (Admirl's Cove, Birh Cove, Fig. 5. Comprison ISI in periwinkles ( Littorin littore) surveyed t sites in Hlifx Hrbour in 1996 (Covert 1997) nd 2006 (this work).

7 Persistene of Imposex nd Intersex in Atlnti Cnd thn tht mesured t Sherwter (42 ng of TBT-Sn/g), nvl bse where three lrge vessels nd over 100 plesure rft dok (Crter et l. 2004) (Fig 6A). Tissue TBT onentrtion mesured in mussels ( Mytilus edulis) tken from the Bedford Yht Club, ner the Admirl's Cove site in 2002 ws 2.5 ng Sn per g (wet weight [w.w.]) (Crter et l. 2004) (Fig. 6B). Sediment levels of TBT n be mesured t sites with reltively fine sediment, but orgnisms suh s mussels nd dogwhelks require hbitt tht inludes orser snd nd solid rok. It is thus diffiult to find sites where TBT onentrtions n be mesured in both sediment nd niml tissue due to different substrte requirements. The Drtmouth Cove site is situted between the Drtmouth Mrine Slips nd the Drtmouth Shipyrds, doking nd refurbishing fility for lrger ships. A B Lotions of smpling sites in Hlifx Hrbour, Nov Soti, Cnd for TBT. Sites surveyed for imposex in nd intersex in in 2006 (this work) shown in reltion to sites where TBT ws nlyzed in sediments in b 2002 (Crter et l. 2004). ites surveyed for imposex in nd intersex in in 2006 (this b work) shown in reltion to sites where TBT ws nlyzed in tissue in 2002 (Crter et l. 2004).The reltively low levels of TBT tissue ontmintion found by Crter et l. (2004) my be prtilly due to the winter smpling period (Deember to Jnury). Uptke of TBT tends to derese in the lte summer to winter, providing time for TBT to be metbolized to dibutyltin nd monobutyltin, so tht onentrtion of these metbolites inrese ompred to TBT in the tissues of ontminted nimls during this time period (St.-Jen et l. 1999).

8 Cory nd Brd The next highest rte of imposex (92%) ws observed t the BIO site, where lrge ships often dok. Fifty perent imposex ws observed t site djent to mjor shipping lne (Ferguson's Cove), nd 19% imposex ws observed t site djent to mjor muniipl sewge outfll (Pt. Plesnt). No imposex ws observed t the referene site (Dunn's Cove), where no known urrent input or historil ontmintion of TBT is evident.

9 Persistene of Imposex nd Intersex in Atlnti Cnd n ompletely lter the struture of n eosystem through their presene or bsene. As first introdued by Pine (1966, 1969), keystone speies is one whose presene is ruil in mintining the orgniztion nd diversity of their eologil ommunities, nd N. lpillus seems to ply this role in intertidl ommunities in nd round Hlifx Hrbour. Severl speies of thid gstropods, of whih N. lpillus is one, hve been shown to ply n importnt predtory role in struturing roky shore ommunities (Lubheno nd Menge 1978; Menge 1983; Menge 1995; Minhinton 1990). It is well doumented tht ertin keystone speies

10 Cory nd Brd Referenes Environmentl problems used by TBT in Frne: Assessment, regultions, prospets. Mr. Environ. Res. : Evlution des risques des à l'emploi des peintures nislissures dns les zenes onhylioles. Rev. Trv. Inst. Pêh. Mrit. : Sptil nd temporl hnges of TBT pollution long the Portuguese ost: Ineffiy of the EEC diretive 89/677. Mr. Pollut. Bull. (6): The distribution nd fte of tributyl tin in the mrine environment, hp. 5 de Mor SJ (ed.), Tributyl tin: Cse study of n environmentl ontminnt. Cmbridge University Press, U.K. Conlusions Aknowledgments TBT effets on the femle genitl system of : A possible inditor of tributyltin pollution. Hydrobiologi. : Reolonistion nd reovery of popultions of dogwhelks (L.) on shores formerly subjet to severe TBT ontmintion. Mr. Pollut. Bull. (7): (Nssriide: Gstropod) s n inditor of tributyltin pollution before nd fter TBT restritions. J. Mr. Bio. Asso.UK. (4): A omprison of the effetiveness of tri-n-butyltin hloride nd five other orgnotin ompounds in promoting the development of imposex in the dogwhelk,. J. Mr. Bio. Asso. UK. : The effets of tributyltin TBT umultion on dult dogwhelks, : Long term field nd lbortory experiments. J. Mr. Bio. Asso.UK. : The deline of the gstropod round southwest Englnd: Evidene for the effet of tributyltin from ntifouling pints. J. Mr. Bio. Asso.UK. : Aumultion of ontminnt metls in mrine sediments of Hlifx Hrbour, Nov Soti: Environmentl ftors nd historil trends. Appl. Geohem. : Geohemil hrteristis of ontminted surfiil sediments in Hlifx Hrbour: Impt of wste dishrge. Cn. J. Erth Si. : Antifouling pints for ship hulls. Cndin Assoition of Pestiide Control Offiils Note 89-02, Ottw, ON, Cnd An ssessment of sediment nd blue mussels ( ) from Atlnti Cnd hrbours: Butyltin nd hevy metl onentrtions nd mussel biomrkers. EPS-5- AR-06-01, Environment Cnd, Atlnti Region Ourrene of orgnotin ompounds in the Cndin quti environment five yers fter the regultion of

11 Persistene of Imposex nd Intersex in Atlnti Cnd ntifouling uses of tributyl tin. Wter Qul. Res. J. Cnd. : Oureny of butyltin speies in sewge nd sludge in Cnd. Si. Totl Environ. : Intertidl biodiversity monitoring s tool for ssessing impts of muniipl mrine pollution. The EMAN Monitor 4(3):3-4. Avilble online t reports/newsletters/monitor/vol_4_num_3/pge3.html (Aessed Deember 5, 2006) Msuliniztion of dogwhelks ( ) nd periwinkles ( ) in Hlifx Hrbour: Monitoring of tributyltin. Honours BS Thesis, Sint Mry's University, Hlifx, Nov Soti Tributyl tin (TBT) pollution in riverine sediments following spill from timber tretment fility in Henderson, New Zelnd. Environ. Tehnol. : Morphologil effets of tributyltin (TBT) in vitro on the genitl system of the mesogstropod (Prosobrnhi). Helgo. Meer. : Persistene nd degrdtion pthwys of tributyltin in freshwter nd esturine sediments. Estur. Cost. Shelf Si. (5): Biodegrdtion of tributyltins (orgnotins) by mrine bteri. Appl. Orgnometl. Chem. : Chnges in butyltin residue onentrtions in mrine sediments of Atlnti Cnd between 1988 nd EPS-5-AR-99-1, Environment Cnd, Atlnti Region The TBT bn: Out of the frying pn nd into the fire? Mr. Pollut. Bull. (3): Widespred reovery of dogwhelks, (L.), from tributyltin ontmintion in the North Se nd Clyde Se. Mr. Pollut. Bull. (3): Reovery in popultions of dogwhelks (L.) suffering from imposex. Mr. Pollut. Bull. (7): Orgnotin ompounds in muniipl wstewter nd sewge sludge: Contmintion, fte in tretment proess nd eotoxiologil onsequenes. Si. Totl Environ. : Fte of tributyltin in sewge sludge tretment. Mr. Environ. Res. : British Prosobrnh Molluss: Their Funtionl Antomy nd Eology. Ry Soiety, London Imposex nd orgnotin body burden in the dog-whelk ( L.) long the Portuguese ost. Appl. Orgnomet. Chem. (1): The use of the dog-whelk,, s n inditor of tributyltin (TBT) ontmintion. J. Mr. Bio. Asso. UK. : Physil ftors, behvior nd intertidl life of. Cndin Biology of Fishes in Nov Soti. : Report of the federl-provinil environmentl ssessment review pnel for the Hlifx-Drtmouth metropolitn wstewter mngement system Orgni hemils in sewge sludges. Si. Totl Environ. : Tributyltin levels in mrine sediments. EPS-5-AR-92-3, Environment Cnd, Atlnti Region Imposex in : A ten yer survey in NW Brittny. Mr. Eol. Prog. Ser. : [online]. [ited 11/ ] Butyltin residues in sediment, fish, fish-eting birds, hrbour porpoise nd humn tissues from the polish ost of the Blti Se. Mr. Pollut. Bull. : Butyltin residues in southern se otters ( ) found ded long liforni ostl wters. Environ. Si. Tehnol. : Community development nd persistene in low roky intertidl zone. Eol. Mono. : Review: Environmentl spets of tributyltin. Appl. Orgnometl. Chem. : Review of the persistene, bioumultion nd toxiity of tributyltin in quti environments in reltion to Cnd's toxi substnes mngement poliy. Wter Qul. Res. J. Cnd. (4): Cndin Environmentl Protetion At priority substnes list ssessment report - non-pestiidl orgnotin ompounds. Deprtment of the Environment, Commeril Chemils Evlution Brnh, Ottw, ON, Cnd Critil pprisl of the evidene for tributyltin-medited endorine disruption in mollusks. Environ. Toxiol. Chem. (1): Components of predtion intensity in the low zone of the New Englnd rok intertidl region. Oeologi (2): Indiret effets in mrine roky intertidl intertion webs: Ptterns nd importne. Eol Mono (1): Mrine TBT ntifouling ontmintion in Irelnd, following legisltion in Mr. Pollut. Bull. (10): Biologil inditors used to mp orgnotin ontmintion in Cork Hrbour, Irelnd. Mr. Pollut. Bull. (2): Ftors influening settlement nd survivl of the brnle, (L.), in

12 Cory nd Brd developing roky intertidl ommunity in Nov Soti, Cnd. MS Oenogrphy, Dlhousie University, 136 pp Imposex in from southern Austrli. Mr. Pollut. Bull. : Imposex in nd intersex in : Interspeifi omprison of two TBT-indued effets nd their geogrphil uniformity. Hydrobiologi. : Orgnotin ntifouling pints nd their lterntives. Appl. Orgnometl. Chem. : Food web omplexity nd speies diversity. Am Nt : A note on trophi omplexity nd speies diversity. Am Nt : Orgnometlli omplexes with biologil moleules. XVI. Endorine disruption effets of tributyltin(iv)hloride on metmorphosis of the sidin lrv. Appl. Orgnometl. Chem. : A bseline survey of dog whelk ( ) imposex in estern Cnd (1995) nd interprettion in terms of tributyltin (TBT) ontmintion. Environ. Tehnol. : Inresing imposex in popultions of (Gstropod: Muriide) in the northwestern Mediterrnen. Mr. Environ. Res. (5): Inidene of imposex in from Port Phillip By (Vitori, Austrli), following 10 yers of regultion on use of TBT. Mr. Pollut. Bull. (10): Further reovery of northest Pifi neogstropods from imposex relted to tributyltin ontmintion. Mr. Pollut. Bull. (3): Sexulity in the Amerin mud snil,. Sy. Pro. Ml. So. Lond. : Butyltin onentrtions in sediments nd blue mussels ( ) of the southern Gulf of St. Lwrene. Cnd. Environ. Tehnol. (2): Hemoyte funtions nd bteril lerne ffeted by TBT nd DBT in the blue mussel. Mr. Eol. Prog. Ser. : b. Very low levels of wterborne butyltins modulte hemoyte funtion in the blue mussel. Mr. Eol. Prog. Ser. : Tributyl tin: The se for virtul elimintion in Cnd. World Wildlife Fund Cnd, Tributyltin exposure uses deresed grnzyme B nd perforin levels in humn nturl killer ells. Toxiology. (2-3): DNA dmge indued by orgnotins on trout-nuleted erythroytes. Appl. Orgnometl. Chem. : Highly persistent butyltins in northern mrine sediments: A long-term thret for the Sgueny Fjord (Cnd). Environ. Toxiol. Chem. (11): Removl of orgnotins during sewge tretment: A se study. Environ. Tehnol. : Reeived: 2 Februry 2007; epted 23 April Butyltin ontmintion in mrine mmmls from north pifi nd Asin ostl wters. Environ. Si. Tehnol. :