, Volume 137, Issue 1, pp 31–50 | Cite as

Renewal mechanisms of buccal armature in Flabellina verrucosa (Nudibranchia: Aeolidida: Flabellinidae)

  • Anna Mikhlina
  • Alexander Tzetlin
  • Elena Vortsepneva
Original paper


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.


Cladobranchia 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.

Ethical approval

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.


  1. Aumüller G, Wilhelm B, Seitz J (1999) Apocrine secretion—fact or artifact? Ann Anat Anatomischer Anzeiger 181:437–446CrossRefPubMedGoogle Scholar
  2. Beedham GE, Trueman ER (1967) The relationship of the mantle and shell of the Polyplacophora in comparison with that of other Mollusca. J Zool 151:215–231CrossRefGoogle Scholar
  3. Beedham GE, Trueman ER (1968) The cuticle of the Aplacophora and its evolutionary significance in the Mollusca. J Zool 154:443–451CrossRefGoogle Scholar
  4. Bracker CE, Ruiz-Herrera J, Bartnicki-Garcia S (1976) Structure and transformation of chitin synthetase particles (chitosomes) during microfibril synthesis in vitro. PNAS 73:4570–4574CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chen C, Copley JT, Linse K, Rogers AD, Sigwart J (2015) How the mollusc got its scales: convergent evolution of the molluscan scleritome. Biol J Linn Soc 114:949–954CrossRefGoogle Scholar
  6. Dilly PN, Nixon M (1976) The cells that secrete the beaks in octopods and squids (Mollusca, Cephalopoda). Cell Tissue Res 167:229–241CrossRefPubMedGoogle Scholar
  7. 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
  8. Haas W (1981) Evolution of calcareous hard-parts in primitive mollusks. Malacologia 21:403–418Google Scholar
  9. Hickman CS (1980) Gastropod radulae and the assessment of form in evolutionary paleontology. Paleobiology 6:276–294CrossRefGoogle Scholar
  10. Hoffmann H (1939) Opisthobranchia. In: Bronn’s KI (ed) Ordn. Tierreichs, vol 3. Akademische Verlagsgesellschaft mbH, LeipzigGoogle Scholar
  11. Hughes RL (1979) Ultrastructure of the buccal mass in juvenile Coryphella salmonacea (Gastropoda: Nudibranchia). J Molluscan Stud 45:289–295Google Scholar
  12. Isarankura K, Runham NW (1968) Studies on the replacement of the gastropod radula. Malacologia 7:71–91Google Scholar
  13. 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
  14. Kingsley RJ, Froelich J, Marks CB, Spicer LM, Todt C (2013) Formation and morphology of epidermal sclerites from a deep-sea hydrothermal vent solenogaster (Helicoradomenia sp., Solenogastres, Mollusca). Zoomorphology 132:1–9CrossRefGoogle Scholar
  15. Kurosumi K (1984) Mechanism of secretion in endocrine glands. Ultrastructure of endocrine cells and tissues. Springer, Berlin, pp 1–11Google Scholar
  16. Mackenstedt U, Märkel K (1987) Experimental and comparative morphology of radula renewal in pulmonates (Mollusca, Gastropoda). Zoomorphology 107:209–239CrossRefGoogle Scholar
  17. Messenger JB, Young JZ (1999) The radular apparatus of cephalopods. Philos Trans R Soc Lond B Biol Sci 354:161–182CrossRefPubMedCentralGoogle Scholar
  18. Mikhlina AL, Vortsepneva EV, Tzetlin AB (2015) Functional morphology of the buccal complex of Flabellina verrucosa (Opisthobranchia, Gastropoda) invertebrate. Zoology 12:175–196Google Scholar
  19. 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
  20. Mischor B, Märkel K (1984) Histology and regeneration of the radula of Pomacea bridgesi (Gastropoda, Prosobranchia). Zoomorphology 104:42–66CrossRefGoogle Scholar
  21. Peters W (1979) Basal bodies in the odontoblasts of the limpet, Patella coerulea L. (Gastropoda). Cell Tissue Res 202:295–301CrossRefPubMedGoogle Scholar
  22. Rinkevich B (1993) Major primary stages of biomineralization in radular teeth of the limpet Lottia gigantea. Mar Biol 117:269–277CrossRefGoogle Scholar
  23. 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
  24. Threadgold LT (1976) The ultrastructure of the animal cell: international series in pure and applied biology, vol 55. Pergamon Press Ltd, OxfordGoogle Scholar
  25. 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
  26. Vortsepneva E, Ivanov D, Purschke G, Tzetlin A (2013) Morphology of the jaw apparatus in 8 species of Patellogastropoda (Mollusca, Gastropoda) with special reference to Testudinalia tesulata (Lottiidae). Zoomorphology 132:359–377CrossRefGoogle Scholar
  27. Vortsepneva E, Ivanov D, Purschke G, Tzetlin A (2014) Fine morphology of the jaw apparatus of Puncturella noachina (Fissurellidae, Vetigastropoda). J Morphol 275:775–787CrossRefPubMedGoogle Scholar
  28. Wiesel R, Peters W (1978) Light and electron-microscopic investigations on radula complex and radula formation of Biomphalaria glabrata Say (=Australorbis gl) (Gastropoda, Basommatophora). Zoomorphologie 89:73–92CrossRefGoogle Scholar
  29. Wolter K (1992) Ultrastructure of the radula apparatus in some species of aplacophoran molluscs. J Molluscan Stud 58:245–256CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Invertebrate Zoology Department, Biological FacultyM. V. Lomonosov Moscow State UniversityMoscowRussia
  2. 2.N. A. Pertsov White Sea Biological StationMoscowRussia

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