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Articles

The fine structure of gametogenesis and somatic cells in the ovotestis of the terrestrial pulmonate slug, Laevicaulis alte (Férussac, 1822)

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Pages 355-372 | Received 24 Jul 2018, Published online: 30 Jun 2019

References

  • Anderson, W.A. & Personne, P. (1967) The fine structure of the neck region of spermatozoa of Helix aspersa. Journal de Microscopie 6, 1033–1042.
  • Anderson, W.A. & Personne, P. (1970) The localization of glycogen in the spermatozoa of various invertebrate and vertebrate species. The Journal of Cell Biology 44, 29–51. doi: 10.1083/jcb.44.1.29
  • Angeloni, L. & Bradbury, J. (1999) Body size influences mating strategies in a simultaneously hermaphroditic sea slug, Aplysia vaccaria. Ethology Ecology and Evolution 11, 187–195. doi: 10.1080/08927014.1999.9522836
  • Barth, R. & Jansen, G. (1960) Über den begriff “Kinoplasma” in der Spermiogenese von Australorbis glabrata olivaceus (Mollusca, Pulmonata, Planorbidae). Memórias do Instituto Oswaldo Cruz 58, 209–228. doi: 10.1590/S0074-02761960000200007
  • Barth, R. & Jansen, G. (1961) Über die Formveränderungen des Golgi-Apparates während der Spermiogenese von Australorbis glabratus olivaceus (Mollusca, Pulmonata, Planorbidae). Memórias do Instituto Oswaldo Cruz 59, 83−114. doi: 10.1590/S0074-02761961000100009
  • Barth, R. & Jansen, G. (1962) Beobachtungen fiber die Entwicklung und Ernährung der Eizellen yon Australorbis glabratus olivaceus (Gastropoda, Pulmonata, Planorbidae). Anais da Academia Brasileira de Ciências 34, 381–389.
  • Bateman, A.J. (1948) Intra-sexual selection in Drosophila. Heredity 2, 349–368. doi: 10.1038/hdy.1948.21
  • Beguelini, M.R., Taboga, S.R. & Morielle-Versute, E. (2013) Ultrastructural characteristics of the spermatogenesis during the four phases of the annual reproductive cycle of the black Myotis bat, Myotis nigricans (Chiroptera: Vespertilionidae). Microscopy Research and Technique 76, 1035–1049. doi: 10.1002/jemt.22264
  • Bhavare, M.K. & Magare, S.R. (2017) Ecology and population studies of land slug, Laevicaulis alte in Shahada region. Journal of Applied and Advanced Research 2, 63–66. doi: 10.21839/jaar.2017.v2i2.58
  • Bing, H.U., Xiao-zhen, Y., Xu-gan, W.U., Wei-ming, T. & Yong-xu, C. (2008) Development of gonad in different body weights of Onchidium struma. Zoological Research 29, 145−151. doi: 10.3724/SP.J.1141.2008.00145
  • Bluemink, J.G. (1967) The subcellular structure of blastula of Lymnaea stagnalis L. (Mollusca) and the mobilization of the nutrient reserve. Ph.D. Thesis, University of Utrecht.
  • Boato, A. & Rasotto, M.B. (1987) Functional protandry and seasonal reproductive cycle in Solatopupa similis (Bruguière) (Pulmonata Chondrinidae), Bolletino di zoologia 54, 119–125. doi: 10.1080/11250008709355570
  • Bouchet, P. & Rocroi, J-P. (2005) Classification and nomenclator of gastropod families. Malacologia 47, 1–397.
  • Buckland-Nicks, J. (1998) Prosobranch parasperm: sterile germ cells that promote paternity? Micron 29, 267–280. doi: 10.1016/S0968-4328(97)00064-4
  • Buckland-Nicks, J. & Chia F-S. (1986) Fine structure of Sertoli cells in three marine snails with discussion on the functional morphology of Sertoli cells in general. Cell and Tissue Research 245, 305–313. doi: 10.1007/BF00213936
  • Charnov, E.L. (1996) Sperm competition and sex allocation in simultaneous hermaphrodites. Evolution and Ecology 10, 457–462. doi: 10.1007/BF01237878
  • Chen, S.H., Xia, L.P., Dahms, H.U., Peng, X. & Ying, X.P. (2015) The ultrastructural characteristics of spermatogenesis in Onchidium struma (Pulmonata: Onchidiidae) and its functional adaptation. Italian Journal of Zoology 82, 1–10.
  • Coggeshall, R.E. (1972) The muscle cells of the follicle of the ovotestis in Aplysia as the probable target organ for bag cell extract. Annales Zoologici 12, 521–523.
  • Cunha, R., Rodrigues, A. & Sousa, H. (1998) The albumen gland as a maturation diagnostic organ in Oxychilus (Drouetia) atlanticus (Stylommatophora, Zontidae). Iberus 16, 75–84.
  • Deshpande, U.D. & Nagabhushanam, R. (1983) Annual reproductive cycle of marine pulmonate, Onchidium verruculatum (Cuvier) and its control by environmental factors. Indian Journal of Marine Sciences 12, 122–124.
  • De Witt, T.J. (1996) Gender contests in a simultaneous hermaphrodite snail: a size advantage model for behavior. Animal Behavior 51, 345–351. doi: 10.1006/anbe.1996.0033
  • Dykstra, M.J. (1993) A Manual of Applied Techniques for Biological Electron Microscopy. Plenum Press, New York.
  • Eckelbarger, K.J. & Blades-Eckelbarger, P. (1989) Structure of the ovotestis and evidence for heterosynthetic incorporation of yolk precursors in the oocytes of the nudibranch mollusk, Spurilla neapolitana. Journal of Morphology 201, 105–118. doi: 10.1002/jmor.1052010202
  • Favard, P. & Carasso, N. (1958) Origine et ultrastructure des plaquettes vitellines de la planorbe. Archives d'anatomie microscopique et de morphologie expérimentale 47, 211–229.
  • Griffond, B. & Bolzoni-Sungur, D. (1986) Stages of oogenesis in the snail, Helix aspersa: cytological, cytochemical and ultrastructural studies. Reproduction, Nutrition and Development 26, 461–474. doi: 10.1051/rnd:19860307
  • Healy, J.M. (2001) Spermatogenesis and oogenesis. In: Barker, G.M. (Ed), The Biology of Terrestrial Molluscs. CABI Publishing, Wallingford, UK, pp. 357–382.
  • Heller, J. (1990) Longevity in molluscs. Malacologia 31, 259–295.
  • Heller, J. (2001) Life history strategies. In: Barker, G.M. (Ed.), The Biology of Terrestrial Molluscs. CABI Publishing, Wallingford, UK, pp. 413–445.
  • Hermann, P.M., Genereux, B. & Wildering, W.C. (2009) Evidence for age-dependent mating strategies in the simultaneous hermaphrodite snail, Lymnaea stagnalis (L.). Journal of Experimental Biology 212, 3164–3173. doi: 10.1242/jeb.030031
  • Horn, A.C.M., Achaval, M. & Zancan, D.M. (2005) The annual reproductive cycle of the snail Megalobulimus abbreviatus (Bequaert, 1948) (Gastropoda, Pulmonata). Brazilian Journal of Biology 65, 459–467. doi: 10.1590/S1519-69842005000300011
  • Jong-Brink, M. De., Boer, H.H., Hommes, T.G. & Kodde, A. (1977). Spermatogenesis and the role of Sertoli cells in the freshwater snail Biomphalaria glabrata. Cell and Tissue Research 181, 37–58. doi: 10.1007/BF00222773
  • Jong-Brink, M. De., Boer, H.H. & Joose, J. (1983) Molluska. In: Adiyodi, K.G. & Adiyodi, R.G. (Eds.), Reproductive Biology of Invertebrates, John Wiley, New York, pp. 297–355.
  • Jong-Brink, M. De., De Wit, A., Kraal, G. & Boer, H.H. (1976) A light and electron microscope study on oogenesis in the fresh water pulmonate slug Biomphalaria glabrata. Cell and Tissue Research 171, 195–219. doi: 10.1007/BF00219406
  • Jong-Brink, M. De., Schot, L.P., Schoenmakers, H.J. & Baergamin Sassen, M.J.M. (1981) A biochemical and quantitative electron microscope study on steroidogenesis in ovotestis and digestive gland of the pulmonate slug Lymnaea stagnalis. General and Comparative Endocrinology 45, 30–38. doi: 10.1016/0016-6480(81)90165-9
  • Joosse, J. & Reitz, D. (1969) Functional anatomical aspects of the ovotestis of Lymnaea stagnalis. Malacologia 9, 101–109.
  • Jordaens, K., Pinceel, J. & Backeljau, T. (2005) Mate choice in the hermaphroditic land snail Succinea putris (Stylommatophora: Succineidae). Animal Behaviour 70, 329–337. doi: 10.1016/j.anbehav.2004.10.021
  • Jörger, K.M., Stöger, I., Kano, Y., Fukuda, H., Knebelsberger, T. & Schrödl, M. (2010) On the origin of Acochlidia and other enigmatic euthyneuran gastropods, with implications for the systematics of Heterobranchia. BMC Evolutionary Biology 10, 323. doi: 10.1186/1471-2148-10-323
  • Kimura, K., Hirano, T., Chiba, S. (2015) Assortative mating with respect to size in the simultaneously hermaphroditic land snail Bradybaena pellucida. Acta Ethologica. 18, 265–268. doi: 10.1007/s10211-014-0211-7
  • Kocot, K.M., Halanych, K.M. & Krug, P.J. (2013) Phylogenomics supports Panpulmonata: opisthobranch paraphyly and key evolutionary steps in a major radiation of gastropod molluscs. Molecular Phylogenetics and Evolution 69, 764–771. doi: 10.1016/j.ympev.2013.07.001
  • Kulkarni, A.B. (1973) The anatomy and histology of the reproductive system of the land slug, Laevicaulis alte. Marathwada University Journal of Sciences 12, 61–69.
  • Leonard, J.L. (2005) Bateman's principle and simultaneous hermaphrodites: a paradox. Integrative and Comparative Biology 45, 856–873. doi: 10.1093/icb/45.5.856
  • Lofts, B. & Bern, H.A. (1972) The functional morphology of steroidogenic tissues. In: Idler, D.R. (Ed.), Steroids in Non-Mammalian Vertebrates. Academic Press, New York, pp. 37–125.
  • Luchtel, D.L. (1972a) Gonadal development and sex determination in pulmonate mollusks Arion circumscriptus. Zeitschrift für Zellforschung 130, 279–301. doi: 10.1007/BF00306943
  • Luchtel, D.L. (1972b) Gonadal development and sex determination in pulmonate mollusks. 1. Arion ater rufus and Deroceras reticulatum. Zeitschrift für Zellforschung 130, 302–311. doi: 10.1007/BF00306944
  • Maekawa, M., Kamimura, K. & Nagano, T. (1996) Peritubular myoid cells in the testis: Their structure and function. Archives of Histology and Cytology 59, 1–13. doi: 10.1679/aohc.59.1
  • Nagabhushanam, R. & Kulkarni, A.B. (1971) Reproductive biology of the land slug, Laevicaulis alte. Rivista di Biologia 64, 15–33.
  • Nakadera, Y., Swart, E.M., Maas, J.P.A., Montagne-Wajer, K., Ter Maat, A. & Koene, J.M. (2015) Effects of age, size, and mating history on sex role decision of a simultaneous hermaphrodite. Behaviour Ecology 26, 232–241. doi: 10.1093/beheco/aru184
  • Nørrevang, A. (1968) Electron microscopic morphology of oogenesis. International Review of Cytology 23, 113–186. doi: 10.1016/S0074-7696(08)60271-5
  • Norton, C.G. & Bronson J.M. (2006) The relationship of body size and growth to egg production in the hermaphroditic freshwater snail, Helisoma trivolvis. Journal of Molluscan Studies 72, 143–147. doi: 10.1093/mollus/eyi057
  • Odiete, W.O. (1982) Fine structural studies on the ovotestis of Archachatina marginata (Swainson) (Pulmonata: Stylommatophora). Malacologia 22, 137–143.
  • O’Donavan, P. & Abraham, M. (1987) Somatic tissue-male germ cell barrier in three hermaphrodite invertebrates: Dugesia biblica (Platyhelminthes), Placobdella costata (Annelida), and Levantina hierosolyma (Mollusca). Journal of Morphology 192, 217–227. doi: 10.1002/jmor.1051920304
  • Ohbayashi-Hodoki, K., Ishihama, F. & Shimada, M. (2004) Body size–dependent gender role in a simultaneous hermaphrodite freshwater slug, Physa acuta. Behavioural Ecology 15, 976–981. doi: 10.1093/beheco/arh101
  • Okamura, F. & Nishiayama, H. (1976) The early development of the tail and the transformation of the shape of the nucleus of the spermatid of the domestic fowl, Gallus gallus. Cell and Tissue Research 169, 345–359. doi: 10.1007/BF00219607
  • Otsuka, C., Rouger, Y. & Tobach, E. (1980) A possible relationship between size and reproductive behavior in a population of Aplysia punctata (Cuvier, 1803). Veliger 23, 159–162.
  • Pal, P. & Hodgson, A.N. (2002) An ultrastructural study of oogenesis in a planktonic and a direct developing species of Siphonaria (Gastropoda: Pulmonata). Journal of Molluscan Studies 68, 337–344. doi: 10.1093/mollus/68.4.337
  • Parivar, K. (1978) A histological survey of gonadal development in Arion ater (Mollusca, Pulmonata). Journal of Molluscan Studies 44, 250–264.
  • Parivar, K. (1980) Differentiation of the Sertoli cells and post reproductive epithelial cells in the hermaphrodite gland of Arion ater (L.) (Mollusca, Pulmonata). Journal of Molluscan Studies 46, 139–147.
  • Quattrini, D. & Lanza, B. (1964) Osservazioni sulla ovogenesi e sulla spermatogenesi di Vaginulus borellianus (Colosi) Mollusca Gastropoda Soleolifera. Bolletino di Zoologia 31, 541–553. doi: 10.1080/11250006409441087
  • Quatrini, D. & Lanza, B. (1965) Ricerche, Sulla biologia di Vernocellidae (Gastropoda-Soliolifera). II. Structuradella gonad ovogenesi e spermatogenesis in Vaginulus borellianus (Colosi) e in Laevicaulis alte (Férussac). Monitore Zoologica Italiano 73, 3–60.
  • Rakshit, S., Chaki, K.K., Sarkar, A.K. & Misra, K.K. (2005) Cytomorphology of ovotestis of a pulmonate mollusk, Achatina fulica. Proceedings of the Zoological Society Calcutta 58, 93–104.
  • Raut, S.K. & Panigrahi, A. (1990) Feeding rhythm in the garden slug Laevicaulis alte (Soleolifera: Veronicellidae). Malacological Review 23, 39–46.
  • Rigby, J.E. (1982) The fine structure of differentiating spermatozoa and Sertoli cells in the gonad of the pond snail, Lymnaea stagnalis. Journal of Molluscan Studies 48, 111–123.
  • Roy, S., Chaki, K.K., Nag, T.C. & Misra, K.K. (2016) Ultrastructure of ovotestis of young and adult of a pulmonate mollusk, Macrochlamys indica (Benson, 1832). Journal of Microscopy and Ultrastructure 4, 184–194. doi: 10.1016/j.jmau.2016.03.001
  • Roy, S., Chaki, K.K., Nag, T.C. & Misra, K.K. (2018) Ultrastructure of gametogenesis in the ovotestis of an estuarine pulmonate slug, Onchidium tigrinum (Stoliczka 1869). Molluscan Research 38, 243–257. doi: 10.1080/13235818.2018.1434605
  • Rustom, R., Saffrich, R., Markovic, I., Walther, P. & Gerdes, H.H. (2004) Nanotubular highways for intercellular organelle transport. Science 303, 1007–1010. doi: 10.1126/science.1093133
  • Sabelli, B. & Sabelli, F.S. (1980) Sexualization of germ cells in Papollifera papillaris (Muller). (Pulmonata, Stylommatophora). Italian Journal of Zoology 14, 19–26.
  • Selmi, M.G., Giusti, F. & Manganelli, G. (1988) The fine structure of the mature spermatozoon of Onchidella celtica (Cuvier) (Mollusca: Gastropoda) and its phylogenetic implications. Journal of Ultrastructure and Molecular Structure Research 99, 107–123. doi: 10.1016/0889-1605(88)90047-X
  • Silva, da R.F., Cubas, J.J.M. & De Moraes J. (2009) Aspectos histológicos das gônadas hermafroditas de Biomphalaria glabrata e Bradybaena similaris (Mollusca, Gastropoda, Pulmonata). Papéis Avulsos de Zoologia 49, 459–466. doi: 10.1590/S0031-10492009003300001
  • Skinner, M.K. & Fritz, I.B. (1985) Testicular peritubular cells secrete a protein under androgen control that modulates Sertoli cell functions. Proceedings of the National Academy of Sciences, USA 82, 114–118. doi: 10.1073/pnas.82.1.114
  • Staib, R. & Ribi, G. (1995) Size-assortative mating in a natural population of Viviparus ater (Gastropoda: Prosobranchia) in Lake Zurich, Switzerland. Journal of Molluscan Studies 61, 237–247. doi: 10.1093/mollus/61.2.237
  • Starke, F.J. (1971) Elektronenmikroskopische Untersuchung der Zwittergonadenacini von Planorbarius corneus L. (Basommatophora). Zeitschrift Zellforsch 119, 483–514. doi: 10.1007/BF00455244
  • Taylor, G.T. & Anderson, E. (1969) Cytochemical and fine structural analysis of oogenesis in the gastropod, llyanassa obsoleta. Journal of Morphology 129, 211–247. doi: 10.1002/jmor.1051290206
  • Terakado, K. (1974) Origin of yolk granules and their development in the snail Physa acuta. Journal of Electron Microscopy 23: 99–106.
  • Till-Bottraud, I., Joly, D., Lachaise, D. & Snook, R.R. (2005) Pollen and sperm heteromorphism: convergence across kingdoms? Journal of Evolutionary Biology 18, 1–18. doi: 10.1111/j.1420-9101.2004.00789.x
  • Tokuyasu, K.T., Peacock, W.J. & Hardy, R.W. (1972) Dynamics of spermiogenesis in Drosophila melanogaster II. Coiling process. Zeitschrift für Zellforschung und mikroskopische Anatomie 127, 492–525. doi: 10.1007/BF00306868
  • Tomiyama, K. (1995) Mate choice in a simultaneously hermaphroditic land slug, Achatina fulica (Stylommatophora: Achatinidae). In: Guerra, A., Rolán, E. & Rocha, F. (Eds), Proceedings of the 12th International Malacological Congress, Vigo 12, pp. 279–280.
  • Tompa, A. (1984) Land snails (Stylommatophora) In: Saleuddin, A.S.M. & Wilbur, K.M. (Eds), The Mollusca, Academic Press, London, Vol. 7, pp. 47–140.
  • van der Wal, U.P. (1974) De mobilizatie van de dooier van Lymnaea stagnalis L. Ph. D. Thesis, University of Utrecht.
  • Yusa, Y. (1996) The effects of body size on mating features in a field population of the hermaphroditic sea hare Aplysia kurodai Baba, 1937. Journal of Molluscan Studies 62, 381–386. doi: 10.1093/mollus/62.3.381

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