Renewal mechanisms of buccal armature in Flabellina verrucosa (Nudibranchia: Aeolidida: Flabellinidae)
The general and fine morphology of the buccal armature and concomitant epithelia in Flabellina verrucosa were examined using light microscopy, cLSM, TEM, and SEM. A 3D-reconstruction of the radular sheath terminal end was constructed as well. Based on the obtained data, we suggest the mechanisms of jaw and radula syntheses for this species. The jaw plate’s growth is provided by the apocrine secretion of the gnathoblasts. There are two primary areas of jaw synthesis: the anterior area is responsible for growth formation of the jaw portion used in the masticatory process, and the posterior area provides the growth of the jaw plate. These types of synthesis (common for both areas) were described in detail for the first time for Gastropoda. The radula growth is provided by the microvillar activity of odontoblasts and membranoblasts. The rachidian tooth is synthesised by a single cell, and the lateral teeth are synthesised by group of 3–5 cells. The tooth formation includes four main stages: (1) tooth mould formation; (2) 90° turn of the tooth mould; (3) chitin accumulation, and (4) tooth maturation. The wide range of synthesis mechanisms is provided by a combination of two factors: the type of secretion and the amount of cells.
KeywordsCladobranchia Ultrastructure Radula Jaws
The authors thank the divers’ team of the N. A. Pertsov White Sea Biological Station and also I. A. Ekimova (Department of Invertebrate Zoology, Biological faculty, Moscow State University) for providing material. Additionally, we are grateful to Dr. I. A. Kosevich and Dr. N. M. Biserova (Moscow State University) for help with different methods of microscopy. We want to thank the two unknown reviewers for most helpful comments on the typescript. The electron microscopy investigations were performed at the User Facilities Centre of Lomonosov Moscow State University and at the Institute for Biology of Inland Waters of the Russian Academy of Sciences. The present study was supported by Grants 16-04-00343 and 15-29-02447 from the Russian Foundation of Basic Research. The sampling trips and transmission electron microscopy investigations were supported by Russian Foundation for Basic Research Grant 15-04-02580 and by Grant of the President MK-6178.2015.4. The scanning electron microscopy investigations were supported by Russian Scientific Foundation Grant 14-50-00029.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
- Ehrlich H, Kaluzhnaya OV, Brunner E, Tsurkan MV, Ereskovsky A, Ilan M, Tabachnick KR, Bazhenov VV, Paasch S, Kammer M, Born R, Stelling A, Galli R, Belikov S, Petrova OV, Sivkov VV, Vyalikh D, Hunoldt S, Wörheide G (2013) Identification and first insights into the structure and biosynthesis of chitin from the freshwater sponge Spongilla lacustris. J Struct Biol 183:474–483CrossRefPubMedGoogle Scholar
- Haas W (1981) Evolution of calcareous hard-parts in primitive mollusks. Malacologia 21:403–418Google Scholar
- Hoffmann H (1939) Opisthobranchia. In: Bronn’s KI (ed) Ordn. Tierreichs, vol 3. Akademische Verlagsgesellschaft mbH, LeipzigGoogle Scholar
- Hughes RL (1979) Ultrastructure of the buccal mass in juvenile Coryphella salmonacea (Gastropoda: Nudibranchia). J Molluscan Stud 45:289–295Google Scholar
- Isarankura K, Runham NW (1968) Studies on the replacement of the gastropod radula. Malacologia 7:71–91Google Scholar
- Kerth K (1983) Radulaapparat und Radulabildung der Mollusken. II: Zahnbildung, Abbau und Radulawachstum Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere 110:239–269Google Scholar
- Kurosumi K (1984) Mechanism of secretion in endocrine glands. Ultrastructure of endocrine cells and tissues. Springer, Berlin, pp 1–11Google Scholar
- Mikhlina AL, Vortsepneva EV, Tzetlin AB (2015) Functional morphology of the buccal complex of Flabellina verrucosa (Opisthobranchia, Gastropoda) invertebrate. Zoology 12:175–196Google Scholar
- Millonig G (1964) Study on the factors which influence preservation of fine structure. In: Symposium on electron microscopy. Consiglio Nazionale delle Ricerche, Rome, p 347Google Scholar
- Salvini-Plawen L, von Steiner G (1996) Synapomorphies and plesiomorphies in higher classification of Mollusca. In: Taylor J (ed) Origin and evolutionary radiation of the mollusca. Oxford University Press, Oxford, pp 29–51Google Scholar
- Threadgold LT (1976) The ultrastructure of the animal cell: international series in pure and applied biology, vol 55. Pergamon Press Ltd, OxfordGoogle Scholar
- Vortsepneva EV, Tzetlin AB (2014) New data on the fine structure of hooks in Clione limacina (Gastropoda, Opistobranchia) and diversity of the jaw apparatus in gastropods. Zoologicheskii Zhurnal 93:466–478Google Scholar