Persistence of Tributyltin-Induced Imposex in Dogwhelks (Nucella lapillus) and Intersex in Periwinkles (Littorina littorea) in Atlantic Canada

Abstract

Abstract Imposex in gastropods such as dogwhelks (Nucella lapillus) is a sexual abnormality that can cause sterility through the superimposition onto females of male sexual characteristics such as a penis homologue and/or vas deferens. Intersex similarly affects periwinkles (Littorina littorea) and is characterized by a phenotypic disturbance of sex determination between gonad and genital tract. A major culprit in causing imposex and intersex in aquatic gastropods is tributyltin (TBT), which is primarily used as a biocidal compound in antifouling paints, but is also present in sewage and wastewater due to industrial use. Since 1989, TBT has been banned in Canada for use on boats under 25 m in length, and in 2003, the ban was extended to include vessels of any length. However, observations of persistent imposex and intersex in marine snails from Halifax Harbour, Nova Scotia, Canada, suggest that current TBT controls are ineffective to eliminate this environmental problem in active ports. Dogwhelk imposex incidence ranged from 19% at the mouth of Halifax harbour to 100% midharbour, while no dogwhelks were found at the harbour head. Dogwhelks from uncontaminated reference sites outside the harbour yielded no cases of imposex. Imposex frequency and Relative Penis Size Index decreased at some of the sites between 1995 and 2006, but imposex frequency increased from 65 to 100% near a container pier, suggesting that TBT from antifouling paint on large (>25 m) vessels like container ships may still be a strong environmental concern in Halifax Harbour. Periwinkles can tolerate higher TBT exposure and can be found where dogwhelks have been extirpated because of TBT contamination. Intersex incidence ranged from 0% outside the harbour to 100% at the head of the harbour at sites where no dogwhelks were found. Intersex indices corresponded with imposex indices where dogwhelks were found, and were relatively high (>2.0) where dogwhelks were absent. Intersex rates and severity remained constant between 1996 and 2006. These data suggest that TBT-induced imposex may be at least partially responsible for the absence of dogwhelks in certain areas of Halifax Harbour. We also examined the impact of the loss of whelks, important predators for dominant mussels, on intertidal community structure and function. Due to the persistence of TBT in sediments and input of TBT into aquatic environments from sources other than vessel antifouling systems, current TBT controls may be of limited effectiveness in minimizing endocrine disruption and population decline in susceptible marine gastropods.