Generalized System of Imposex and Reproductive Failure in Female Gastropods of Coastal Waters of Mainland China
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MARINE ECOLOGY PROGRESS SERIES Vol. 304: 179–189, 2005 Published December 8 Mar Ecol Prog Ser Generalized system of imposex and reproductive failure in female gastropods of coastal waters of mainland China H. H. Shi1, 2,*, C. J. Huang1, S. X. Zhu1, X. J. Yu1, W. Y. Xie1 1Institute of Marine Biology, Shantou University, Shantou 515063, PR China 2Department of Environmental Sciences, East China Normal University, Shanghai 200062, PR China ABSTRACT: We investigated the occurrence of imposex in gastropods from the coastal waters of mainland China from November 1999 to July 2004. Imposex was found in 30 species from 8 families, and was recorded in 20 species for the first time. In addition to the already known phenotypes of imposex expression in Cantharus cecillei, we also found aborted egg capsules in specimens with a split ventral channel (stage and type classification: S6c*) and various extensions of the proximal vas deferens (PVD). The PVD went up to or passed by the vaginal opening, and then it stopped or continued along the capsule gland. In imposex females, the penis shape and the development of the vas deferens were similar to those of the male of the same species. The morphological expressions of imposex showed diverse stages and types. Reproductive failure of females occurred in 13 species. The results suggest that imposex is widespread and severe in the coastal waters of China. Based on our aims of ecological and morphological significance, a typical imposex classification could be further generalized for all 30 species by adding S6c(*) and 2 subdivisions of the PVD. The generalized scheme was also ascertained to be valid for several morphological variations of imposex in previous work. Sterility at S6c(*) was proven to be due to the infolding of the capsule gland wall. We thus summed up 4 mechanisms of sterility (a, b, c and *) in females. Furthermore, it was shown that the normal structure of the male genital system also affected the morphological expressions of imposex to some degree, which we referred to as ‘effect of male structure’. Finally, we put forward a general classification scheme of imposex with an integrated system of aims, criteria, stages, types (subtypes), pathways and mechanisms of imposex. KEY WORDS: Imposex · Gastropod · Sterility · Mainland China Resale or republication not permitted without written consent of the publisher INTRODUCTION 1999, Horiguchi et al. 2000; see Appendix 1, www.int- res.com/articles/suppl/m304p179_app.pdf). However, Imposex is the occurrence of male sex organs such as on a worldwide scale, there is still a requirement to a penis and vas deferens in female gastropods (Smith extend the scope of studies to include more tropical 1971). This masculinization can lead to reproductive forms (Gibbs & Bryan 1996). failure in females and even to the extinction of A number of species show diverse morphological populations (Gibbs & Bryan 1986). Imposex is mainly expressions of imposex. Fioroni et al. (1991) proposed induced by organotin compounds used as biocides in an imposex classification scheme to outline these antifouling paints (Smith 1981a,b,c, Bryan et al. 1987, expressions based on the presence of a penis, the 1988). To date, more than 170 species of gastropods, extension of the vas deferens and malformations of the represented by 28 families, have been shown to be pallial oviduct in 69 species. The scheme has been affected by imposex (Fioroni et al. 1991, deFur et al. continuously modified (Oehlmann et al. 1991, 1992, *Email: [email protected] © Inter-Research 2005 · www.int-res.com 180 Mar Ecol Prog Ser 304: 179–189, 2005 1996, Stroben et al. 1992). In the typical scheme at the typical scheme, a penis is regarded as a conspicu- present, imposex expressions are classified into ous masculine character and the complete penis will 7 stages, with 3 types (a, b, c) in the first 3 stages and be formed at least in Stage 4. However, sterility may Stage 5, and 2 types in Stages 4 and 6. occur in females of N. lapillus without formation of a This scheme is generally valid for imposex descrip- penis (Huet et al. 1996, Barreiro et al. 1999). tions in most prosobranch species and is widely used Such conspicuous variations usually cause confusion (Kohn & Almasi 1993, Minchin et al. 1997, Bech 2002). when classifying the morphological expressions of However, since the characters of imposex show widely imposex. It is sometimes difficult to distinguish the inter-specific, intra-specific and geographical differ- stages in some species (Power & Keegan 2001). For ences (Fioroni et al. 1991), this typical imposex scheme example, Hexaplex trunculus with aborted egg will probably fail to cover all morphological variations. capsules is still classified as Stage 5 (Axiak et al. 1995). According to the references available, it is not appro- To make the identification easy, several schemes are priate for several of the main types of morphological proposed for specific species, based on different expressions. criteria (Axiak et al. 1995, Barreiro et al. 1999, Mensink Firstly, aborted egg capsules may occur in Nassarius et al. 2002). For example, Barreiro et al. (1999) reticulatus (Buccinidae), even without any external proposed a specific scheme for DS in Nucella lapillus signs of vulva blockage by vas deferens proliferation solely based on vas deferens development instead of (Huet et al. 1995, Barreiro et al. 2001, Barroso et al. vas deferens and penis development in the typical 2002). In Stage 4, the vas deferens develops from the scheme. base of the penis up to the vaginal opening (S4), or Subsequently, the variability in the classification passes by the vaginal opening and runs into the ventral makes the assessment of imposex problematic when channel of the capsule gland (S4*). Stroben et al. (1992) comparing different investigations if different values first distinguished S4* based on findings in N. reticula- of the vas deferens sequence index (VDSI) are used for tus and regarded it as the end of imposex development the same expression (Ruiz et al. 2005). For example, in this species. However, later surveys suggested that the VDSI of Nassarius reticulatus at S4* has been sterility of N. reticulatus females appears to be a com- computed as 4.0, 4.5 and 5.0 by different researchers mon phenomenon (Huet et al. 1995, Barreiro et al. (Stroben et al. 1992, Barreiro et al. 2001, Barroso et al. 2001, Barroso et al. 2002). 2002). Secondly, aborted egg capsules are often present in In addition, the mechanisms of sterility are still Hexaplex trunculus with a ventrally split pallial ambiguous in Nassarius reticulatus and Hexaplex oviduct (Terlizzi et al. 2004). According to the typical trunculus. The classification is just based on the scheme, a split pallial oviduct prevents copulation due hypothesis that the degree of imposex will be to the open bursa copulatrix or egg capsule formation upgraded along the scheme. Therefore, if the mech- as a consequence of the open capsule gland. There- anisms are not clearly revealed, it is hard to classify the fore, it was argued that aborted egg capsules cannot expression of imposex reasonably. To date, 2 mecha- be formed and consequently no S6c stage should exist. nisms have been described (Gibbs & Bryan 1996, However, the reports of aborted egg capsules in Oehlmann et al. 1998). One mechanism is the blockage H. trunculus resemble Stage 6 in Nucella lapillus of the vulva by vas deferens tissue or the replacement (Gibbs & Bryan 1986, Terlizzi et al. 2004). of the vulva by the prostate, the other is the presence of Thirdly, various extensions of the proximal vas a longitudinal split in the capsule gland of the adult. It deferens (PVD) occur in several species such as is assumed that aborted egg capsules can only be Lepsiella scobina, Nassarius reticulatus, Neptunea formed in the first case. However, neither mechanism antiqua and Cantharus cecillei (Stewart et al. 1992, above completely fits the formation of aborted egg Power & Keegan 2001, Barroso et al. 2002, Shi et al. capsules in N. reticulatus or H. trunculus, and new 2005). In the typical scheme, the PVD either joins the mechanisms have not yet been revealed. vaginal opening or passes by it and enters the capsule Gibbs & Bryan (1996) supposed that the male gland. In some species, however, the PVD also extends structure provides important clues as to the net effect laterally after joining the vaginal opening, or passes by of imposex when the female individual is promoted to the vaginal opening and just ends in the posterior an advanced stage. Muricidae are prone to sterility section of the pallial cavity (Fioroni et al. 1991). because the male tract follows the same path within Finally, a penis may be lacking and yet, vas deferens the mantle cavity as that of the female tract. The pallial formation may be weak in imposex-affected females of vas deferens of males in other groups is parallel to the Nucella lapillus. This phenomenon was first reported extension of the oviduct in females. In these cases, the in a restricted area in Southeast England by Gibbs vas deferens of imposex individuals contacts the (1993) who called it the Dumpton Syndrome (DS). In oviduct some distance behind the genital papilla and Shi et al.: Imposex in gastropods from China 181 does not interfere with copulation or capsule release. and analyzed using Axio Vision 3.0. One hundred and However, sterility still occurs in families other than sixty specimens for scanning electron micrographs Muricidae such as Buccinidae (Barreiro et al. 2001, Shi were fixed in glutaraldehyde directly after narcotiza- et al. 2005). Therefore, it is not clear whether sterility tion in MgCl2. Samples were dehydrated via a graded can be predicted from the male structure. ethanol series, critical point dried and coated with Currently, these variations give rise to some confu- gold.