Reproductive impairment and intersexuality inGomphina veneriformis(Bivalvia: Veneridae) by the tributyltin compound

Abstract

A well-established xenoandrogen, tributyltin (TBT) causes sexual interferences in various animal models including gastropods. In bivalves, the disrupting effects of TBT on reproduction are largely unevaluated. In this study, we carried out a test on reproduction of the bivalve (Gomphina veneriformis) affected by TBT (0.4, 0.6, and 0.8 μg L −1 ). The experimental period was 36 weeks, starting in October during the inactive stage of the clam's reproductive cycle. The sex ratio (F:M) was 1:1.00 in the control group but changed to 1:1.37 in all the exposed groups with 0.8 μg L −1 TBT, leading to significantly higher values in male (1:1.54; P = 0.009). Gonadal maturity (ripe stage frequency) of males in the exposure groups was higher than females. The gonad index (GI) of females significantly decreased when exposed to 0.6 and 0.8 μg L −1 TBT. The prevalence of intersex was significantly different between males and females in all exposure groups, which became significantly different (P < 0.001) after 20 weeks. A high prevalence of intersex (67.80%) was detected in 0.8 μg L −1 after 36 weeks. These results suggest that TBT, a xenoandrogen, may lead to skewed sex ratio toward males, inhibit sexual maturation of the females, and also induce intersex in G. veneriformis as an imposex of gastropods. Therefore, reproductive indicators (sex ratio, gonadal development, and intersexuality) of bivalves may be used as useful bioindicators in monitoring marine pollution by TBT compounds.

Dynamics of nuclear receptor gene expression during Pacific oyster development

“…Many of the effects of environmental estrogens are known to be mediated through interaction with NRs [ 15 – 18 ]. Tributyltin (TBT), an organotin and an additive in antifouling paints for boats, has been shown to cause imposex, (superimposition of male organs on females) in > 20 gastropod species [ 19 ] as well as developmental failure and reproduction impairment in bivalves [ 20 – 23 ]. TBT has been identified as a xenobiotic ligand for vertebrate and gastropod NRs [ 24 – 26 ] and a link between NRs and TBT-mediated disruption has been proposed [ 26 – 28 ].…”

Endocrine disruption and altered sexual development in aquatic organisms: an invertebrate perspective

“…Computer predictions confirm the potential for RXR to bind 9-cis retinoic acid and TBT (with, it is hypothesized, corresponding effects on development of oyster larvae) supporting the concept that these NRs could be an important part of the mode of action of some EDC in invertebrates. PPAR and Gonadotrophin Releasing Hormone (and its receptor) are amongst other contenders for a role in imposex development in snails along with inhibition, by TBT, of testosterone-transforming aromatase (Spooner et al ., 1991; Castro et al ., 2007; Pascoal et al ., 2013).…”

“…Synergistic and antagonistic interactions between oestrogenic and androgenic EDC are feasible in nature and can cause complications in the interpretation of intersex levels and sex ratiosfor example in S. plana collected at high TBT sites (discussed above), and in similarly exposed soft shell clams Mya arenaria (Linnaeus, 1758) (Gagné et al, 2006) and mussels Mytilus galloprovincialis (Lamarck, 1819) (Ortiz-Zarragoitia & Cajaraville, 2010). Reproductive impairment (lower Gonadal Index), skewed sex ratios in favour of males, and elevated incidence of intersex (in both females and males) has also been observed in the venerid bivalve Gamphina veneriformis (Lamarck, 1818) as a result of prolonged exposure in the laboratory to elevated TBT levels (0.4-0.8 μg l −1 ) during early gonadal development (Park et al, 2015). Overall intersex frequencies in 'control' G. veneriformis were ∼4%, rising to 31% at high TBT exposure (similar ranges to incidence levels in S. plana from UK estuaries).…”

Sex Determining Mechanisms in Bivalves

“…Relatively little information exists in the literature on the effects of environmental pollutants on bivalve sex determination and differentiation, or reproductive patterns generally (e.g., Gauthier-Clerc et al 2002; Gagné et al 2003;Park et al 2015). However, the complexity of cellular processes involved in sex change and/or gonad differentiation and maturation, certainly provide an opportunity for chemical interference in the pathways leading to the development of females or males.…”

“…However, the complexity of cellular processes involved in sex change and/or gonad differentiation and maturation, certainly provide an opportunity for chemical interference in the pathways leading to the development of females or males. Indeed, several pollutants, such as heavy metals, organophosphates and organochlorines, are known to interfere with the natural role of hormones and consequently affect sex determination, gonad morphology, gametogenesis, and reproduction in molluscs (Park et al 2015). One infamous example is tributyltin (TBT), an organotin compound that has been largely used as a biocide in antifouling agents for boats, and which is now well-established as a xenoandrogen that skews sex ratios toward males in both wild and reared populations of several mollusc species, including bivalves (Table 1).…”