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Does the Histological Structure of Spermoviduct and Free Oviduct Correspond with the Reproductive Mode in Clausiliids (Gastropoda: Pulmonata: Baleinae)?

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Does the Histological Structure of Spermoviduct and Free Oviduct Correspond with the Reproductive Mode in Clausiliids (Gastropoda: Pulmonata: Baleinae)? Folia Malacol. 22(3): 193–199 http://dx.doi.org/10.12657/folmal.022.015 DOES THE HISTOLOGICAL STRUCTURE OF SPERMOVIDUCT AND FREE OVIDUCT CORRESPOND WITH THE REPRODUCTIVE MODE IN CLAUSILIIDS (GASTROPODA: PULMONATA: BALEINAE)? TOMASZ K. MALTZ1*, ANNA SULIKOWSKA-DROZD2, Izabela JędrzeJowska3 1Museum of Natural History, University of Wrocław, Sienkiewicza 21, 50-335 Wrocław, Poland (e-mail: [email protected]) 2Department of Invertebrate Zoology and Hydrobiology, University of Łódź, Banacha 12/16, 90-237 Łódź, Poland 3Department of Animal Developmental Biology, Institute of Experimental Biology, University of Wrocław, Sienkiewicza 21, 50-335 Wrocław, Poland *corresponding author ABSTRACT: Spermoviduct and free oviduct of four species of Baleinae door snails of different reproductive strategy: Laciniaria plicata (oviparity), Vestia gulo (egg retention), Alinda biplicata and Vestia turgida (viviparity), were histologically examined. The spermoviduct contains three partly connected canals: autospermiduct, allospermiduct and oviduct. Their walls are built of pseudostratified epithelium which is composed of large, columnar cells and small, much thinner, supporting cells with the apical surface provided with cellular processes. The free oviduct includes two partly connected canals: oviduct and allospermiduct, with their walls also built of pseudostratified epithelium. Both morphology and secretory activity of epithelial cells are very similar in viviparous and oviparous forms. KEY WORDS: Clausiliidae, reproductive system, Alinda, Laciniaria, Vestia, land snails INTRODUCTION The Baleinae are one of the five subfamilies of specific differences in their reproductive strategies. European clausiliids; they include seven genera with Four species are oviparous: Bulgarica cana, Balea sta- 54 species (NORDSIECK 2007). Till now, life cycles of bilis, Laciniaria plicata and Vestia ranojevici, three: Balea nine Baleinae species (ca. 17% of all species) have fallax, Vestia gulo and V. elata, retain their eggs for a been studied partly or completely (FRÖMMING 1954, shorter or longer time, while another three: Alinda bi- PIECHOCKI 1982, BAUR A. 1990, BAUR B. 1994, WIRTH plicata, Balea perversa and Vestia turgida, are viviparous et al. 1997, MARZEC 2006, MALTZ & SULIKOWSKA- (lecitotrophic viviparity sensu BLACKBURN 1999 or DROZD 2008, 2011, 2012, 2014, SULIKOWSKA-DROZD ovoviviparity sensu TOMPA 1984 and HELLER 2001). 2008, 2009, SULIKOWSKA-DROZD & MALTZ 2012a, b, The anatomy of the reproductive system of most 2013, SULIKOWSKA-DROZD et al. 2012, 2013). Based Baleinae is well known, and data on its structure on laboratory and field observations, it was shown are mainly presented in the systematic and/or phy- that the animals are iteroparous, long-lived, with logenetic context (e.g. STEENBERG 1914, LIKHAREV determinate growth (shell growth terminates with 1962, HUDEC 1963, LUPU 1980, SCHILEYKO 2000, completion of the closing apparatus) and delayed NORDSIECK 2007), whereas information on the his- reproductive maturation (reproductive system be- tological structure of clausiliid reproductive system comes morphologically fully developed 4–5 months is scanty. There are no published comparative data after shell growth completion). There are inter- on the histological structure of the reproductive sys- 194 Tomasz K. Maltz, Anna Sulikowska-Drozd, Izabela Jędrzejowska tem of closely related species with different repro- ed Baleinae was reflected in the histological structure ductive strategies. STEENBERG’s (1914) paper, pub- of their reproductive system. We hypothesised that lished one hundred years ago, is still the main source the different reproductive strategies demand different of information on the histology of clausiliid repro- physiological adaptations, for instance the possibility ductive system. The histological structure presented of gas exchange for developing embryo in viviparous there is based on studies on Cochlodina laminata and species. It is likely that physiological differences are Macrogastra ventricosa – oviparous representatives of expressed in the histology by increased number or Alopiinae and Clausiliinae, respectively. The present activity of certain cell types. Among invertebrates knowledge of the histological structure of the clausil- such physiological modifications in the epithelia of iid reproductive organs is not much greater than that female reproductive system have been reported (e.g. presented by STEENBERG (1914), since the same data WEYGOLDT 1969, FARLEY 1998, JędrzeJowska et are cited in LIKHAREV’s (1962) monograph, while al. 2013). In gastropods data concerning this issue the information in NORDSIECK’s (1966, 1985, 2007) are lacking. Since dissection of egg-filled reproduc- papers is enigmatic and pertains to anatomy rather tive systems of viviparous/egg retaining Baleinae than histology. The recent studies on the histology of (SULIKOWSKA-DROZD 2009, MALTZ & SULIKOWSKA- the reproductive system of Ruthenica filograna – sub- DROZD 2012) corroborated STEENBERG’s (1914) family Clausiliinae (szybIak & Gabała 2013) cor- observation that the eggs were retained in a pocket, roborate STEENBERG’s (1914) observations, especial- formed by the lower part of the spermoviduct and ly regarding the structure of spermoviduct and free the free oviduct of clausiliids, special attention was oviduct in the representatives of the subfamily. paid to these two organs. The objective of this paper was to check if the di- versity of reproductive strategies among closely relat- MATERIAL AND METHODS The studies were conducted in 2010–2011 and material was dehydrated in a graded alcohol series included four species of different reproductive strat- and xylene, embedded in paraffin (Paraplast Plus egies: Laciniaria plicata (oviparity), Vestia gulo (egg with 8% DMSO) and cut on a rotational microtome retention), V. turgida (viviparity) and Alinda biplica- into 7 μm thick sections (serial sections attached ta (viviparity), from the laboratory cultures of the to hot microscopic slides). Following rehydration, Natural History Museum, University of Wrocław the slides with sections were stained with Delafield and the Department of Invertebrate Zoology and hematoxylin and 25% aqueous solution of eosin Hydrobiology, University of Łódź. Five adult, sexual- (ZAWISTOWSKI 1986), dehydrated, cleared and cov- ly mature individuals of each species were dissected erslipped with DPX mounting medium for light mi- in the spring of 2010. In the case of viviparous/egg croscope observations (Olympus BHS). Two organs: retaining species only specimens with no embryos spermoviduct and free oviduct, were subjected to in the reproductive system were used. detailed histological analysis focused on the struc- The reproductive systems were obtained with- ture of the lining epithelium. The same acronyms out gonads from animals killed in boiling water for the specific structures were used throughout the (NORDSIECK 2007) and fixed in Bouin liquid. The text and Figures 1–3. RESULTS AND DISCUSSION The main organs of the Baleinae reproductive sys- SPERMOVIDUCT tem are typical of hermaphroditic Stylommatophora (NORDSIECK 1985, GÓMEZ 2001) (Fig. 1A). Spermo- In all four analysed species the spermoviduct is viduct (so) and free oviduct (fov) were regarded as internally divided into three partly connected canals especially important for the comparative analysis of (Fig. 1B) two of which are located close to the pros- the organs and structures of species with different tate. This confirmsS TEENBERG’s (1914) observation reproductive strategies, as these organs provide a that the spermoviduct (so) is composed of three space for long-term storage of developing embryos parts, separated by incomplete partitions: 1. large, in viviparous species, while in oviparous snails they mucous canal (in this report referred to as oviduct; serve only as a channel for transportation of eggs ov); 2. narrow canal (= allospermiduct; als) and 3. towards the genital orifice. seminal canal (= autospermiduct; aus), to whose Histological structure of reproductive system vs. reproductive mode in clausiliids 195 Fig. 1. Anatomical and histological structure of reproductive system of Alinda biplicata (Ab), Laciniaria plicata (Lp), Vestia gulo (Vg) and V. turgida (Vt): A – schematic drawing of the reproductive system, B – section at spermoviduct level, C – section at free oviduct level; a – atrium, als – allospermiduct, aus – autospermiduct, bc – bursa copulatrix, c – car- refour, dh – hermaphroditic duct, fov – free oviduct, ga – albumen gland, gm – mucus gland, ov – oviduct, p – penis, pr – prostate, so – spermoviduct, vd – vas deferens groove the prostate (pr) glandular tubules open. The FREE OVIDUCT three canals serve to transport three groups of gam- etes: oviduct – eggs, allospermiduct – allosperm, au- In all four species the free oviduct, externally un- tospermiduct – autosperm. According to NORDSIECK divided, is internally divided into two, connected ca- (1985), the tripartite structure makes the reproduc- nals: oviduct (ov) and allospermiduct (als) (Fig. 1C). tive system semitriaulic. The division into three ca- The allospermiduct is formed by a distinct fold which nals is observed both in the egg retaining/viviparous partly separates the main lumen of the organ from A. biplicata, V. gulo and V. turgida and in the oviparous four sinuses built by folded epithelium; this is dis- L. plicata. tinctly visible both in the egg-retaining/viviparous A. 196 Tomasz K. Maltz, Anna Sulikowska-Drozd, Izabela Jędrzejowska
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