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

Zoomorphology volume 137, pages31–50(2018)Cite this article

Abstract

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.

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References

  1. Aumüller G, Wilhelm B, Seitz J (1999) Apocrine secretion—fact or artifact? Ann Anat Anatomischer Anzeiger 181:437–446

    Article  PubMed  Google 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 151:215–231

    Article  Google Scholar 

  3. Beedham GE, Trueman ER (1968) The cuticle of the Aplacophora and its evolutionary significance in the Mollusca. J Zool 154:443–451

    Article  Google 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 73:4570–4574

    CAS  Article  PubMed  PubMed Central  Google 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 114:949–954

    Article  Google Scholar 

  6. Dilly PN, Nixon M (1976) The cells that secrete the beaks in octopods and squids (Mollusca, Cephalopoda). Cell Tissue Res 167:229–241

    CAS  Article  PubMed  Google 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 183:474–483

    CAS  Article  PubMed  Google Scholar 

  8. Haas W (1981) Evolution of calcareous hard-parts in primitive mollusks. Malacologia 21:403–418

    Google Scholar 

  9. Hickman CS (1980) Gastropod radulae and the assessment of form in evolutionary paleontology. Paleobiology 6:276–294

    Article  Google Scholar 

  10. Hoffmann H (1939) Opisthobranchia. In: Bronn’s KI (ed) Ordn. Tierreichs, vol 3. Akademische Verlagsgesellschaft mbH, Leipzig

    Google Scholar 

  11. Hughes RL (1979) Ultrastructure of the buccal mass in juvenile Coryphella salmonacea (Gastropoda: Nudibranchia). J Molluscan Stud 45:289–295

    Google Scholar 

  12. Isarankura K, Runham NW (1968) Studies on the replacement of the gastropod radula. Malacologia 7:71–91

    Google Scholar 

  13. Kerth K (1983) Radulaapparat und Radulabildung der Mollusken. II: Zahnbildung, Abbau und Radulawachstum Zoologische Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere 110:239–269

    Google 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 132:1–9

    Article  Google Scholar 

  15. Kurosumi K (1984) Mechanism of secretion in endocrine glands. Ultrastructure of endocrine cells and tissues. Springer, Berlin, pp 1–11

    Google Scholar 

  16. Mackenstedt U, Märkel K (1987) Experimental and comparative morphology of radula renewal in pulmonates (Mollusca, Gastropoda). Zoomorphology 107:209–239

    Article  Google Scholar 

  17. Messenger JB, Young JZ (1999) The radular apparatus of cephalopods. Philos Trans R Soc Lond B Biol Sci 354:161–182

    Article  PubMed Central  Google Scholar 

  18. Mikhlina AL, Vortsepneva EV, Tzetlin AB (2015) Functional morphology of the buccal complex of Flabellina verrucosa (Opisthobranchia, Gastropoda) invertebrate. Zoology 12:175–196

    Google 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 347

  20. Mischor B, Märkel K (1984) Histology and regeneration of the radula of Pomacea bridgesi (Gastropoda, Prosobranchia). Zoomorphology 104:42–66

    Article  Google Scholar 

  21. Peters W (1979) Basal bodies in the odontoblasts of the limpet, Patella coerulea L. (Gastropoda). Cell Tissue Res 202:295–301

    CAS  Article  PubMed  Google Scholar 

  22. Rinkevich B (1993) Major primary stages of biomineralization in radular teeth of the limpet Lottia gigantea. Mar Biol 117:269–277

    Article  Google 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 29–51

    Google Scholar 

  24. Threadgold LT (1976) The ultrastructure of the animal cell: international series in pure and applied biology, vol 55. Pergamon Press Ltd, Oxford

    Google 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 93:466–478

    Google 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 132:359–377

    Article  Google Scholar 

  27. Vortsepneva E, Ivanov D, Purschke G, Tzetlin A (2014) Fine morphology of the jaw apparatus of Puncturella noachina (Fissurellidae, Vetigastropoda). J Morphol 275:775–787

    Article  PubMed  Google 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 89:73–92

    Article  Google Scholar 

  29. Wolter K (1992) Ultrastructure of the radula apparatus in some species of aplacophoran molluscs. J Molluscan Stud 58:245–256

    Article  Google Scholar 

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Acknowledgements

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.

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Affiliations

  1. Invertebrate Zoology Department, Biological Faculty, M. V. Lomonosov Moscow State University, Leninskie Gory 1/12, 119234, Moscow, Russia

    Anna Mikhlina, Alexander Tzetlin & Elena Vortsepneva

  2. N. A. Pertsov White Sea Biological Station, Leninskie Gory 1/12, 119234, Moscow, Russia

    Anna Mikhlina & Alexander Tzetlin

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  1. Anna Mikhlina
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  2. Alexander Tzetlin
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  3. Elena Vortsepneva
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Correspondence to Anna Mikhlina.

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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.

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Mikhlina, A., Tzetlin, A. & Vortsepneva, E. Renewal mechanisms of buccal armature in Flabellina verrucosa (Nudibranchia: Aeolidida: Flabellinidae). Zoomorphology 137, 31–50 (2018). https://doi.org/10.1007/s00435-017-0370-y

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Keywords

  • Cladobranchia
  • Ultrastructure
  • Radula
  • Jaws