Skip to main content
Log in

Formation of buccal armature of Cadlina laevis (Linnaeus, 1767) (Nudibranchia, Gastropoda)

  • Original Paper
  • Published:
Zoomorphology Aims and scope Submit manuscript

A Correction to this article was published on 07 December 2022

This article has been updated

Abstract

The features of the buccal armature’s morphology and formation process may have phylogenetic significance, be adaptive to the feeding strategy or both. The monophyletic order of gastropods—Nudibranchia—has various feeding strategies and diversified morphology of the buccal armature. That makes nudibranch molluscs a suitable model group for studying the structure and synthesis of the buccal armature. Using methods of micro-CT, light microscopy, SEM, TEM and computer-based 3D-reconstruction we describe for the first time the fine morphology and the formation mechanism of the buccal armature for doridacean nudibranchs on the example of Cadlina laevis (Linnaeus, 1767). The labial cuticle of C. laevis lies on the ventrolateral sides of the buccal cavity. That differs significantly from the case of cladobranchs and other gastropods, whose jaws typically lie dorsally or dorsolaterally. The labial cuticle of C. laevis is a unified matrix with solitary rodlets. A single cell forms each rodlet. This synthesis mechanism is common for molluscan jaw structures containing solitary elements (rodlets). The broad radula of C. laevis folds within the U-shaped radular sac. The connective-tissue collostyle is located above the radular sac and likely prevents the radula from creasing, as was previously described for other Euthyneura with broad radulae. Also, the formation zone of the radula in C. laevis divides into two parts to increase the synthesis surface. That is also specific to broad rhipidoglossan radulae of vetigastropods and neritimorphs. However, the formation of the radular tooth by a few odontoblasts, described earlier for euthyneuran molluscs, remains in C. laevis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Change history

References

  • Brace R (1983) Observations on the morphology and behaviour of Chilina fluctuosa Gray (Chilinidae), with a discussion on the early evolution of pulmonate gastropods. Phil Trans R Soc Lond B, Bio Sci 300(1101):463–491

    Article  Google Scholar 

  • Carriker MR, Bilstad NM (1946) Histology of the alimentary system of the snail Lymnaea stagnalis appressa Say. Trans Am Microsc Soc 65(3):250–275

    Article  CAS  Google Scholar 

  • Curtis SK, Cowden RR (1977) Ultrastructure and histochemistry of the supportive structures associated with the radula of the slug, Limax maximus. J Morphol 151(2):187–211

    Article  CAS  Google Scholar 

  • Dayrat B, Tillier S (2002) Evolutionary relationships of euthyneuran gastropods (Mollusca): a cladistic re-evaluation of morphological characters. Zool J Linn Soc 135(4):403–470

    Article  Google Scholar 

  • Dennis MM, Molnár K, Kriska G, Lőw P (2021) Mollusca: Gastropoda. In: LaDouceur EEB (ed) Invertebrate histology. Wiley-Blackwell, Hoboken, NJ, pp 87–132

    Chapter  Google Scholar 

  • Evans C, Rosen S, Kupfermann I, Weiss K, Cropper E (1996) Characterization of a radula opener neuromuscular system in Aplysia. J Neurophysiol 76(2):1267–1281

    Article  CAS  Google Scholar 

  • Fahey SJ (2004) A new species of Trapania (Nudibranchia: Gonodorididae) from Western Australia with comparisons to other Indo-West Pacific Trapania. Zootaxa 514(1):1–12

    Article  Google Scholar 

  • Fischer MA, Cervera JL (2005) Baptodoris peruviana (D’Orbigny, 1837) Comb Nov an alternative taxonomic placement for Doris peruviana (Gastropoda: Nudibranchia: Doridoidea). J Conchol 38(5):513–528

    Google Scholar 

  • Fretter V (1939) XXII—The structure and function of the alimentary canal of some tectibranch molluscs with a note on excretion. Earth Env Sci Trans R Soc Edinburgh 59(3):599–646

    Google Scholar 

  • Fretter V, Graham A (1949) The structure and mode of life of the Pyramidellidae, parasitic opisthobranchs. J Mar Biol Assoc UK 28(2):493–532

    Article  Google Scholar 

  • Fretter V, Graham A (1962) British prosobranch molluscs. Their functional anatomy and ecology. Ray Society, London, p xvi+755

  • Ghose KC (1963) The alimentary system of Achatina fulica. Trans Am Microsc Soc 82(2):149–167

    Article  Google Scholar 

  • Gosliner TM (1994) Gastropoda: Opisthobranchia. In: Harrison FW, Kohn AJ (eds) Microscopic Anatomy of Invertebrates, vol 5. Mollusca I. Wiley-Liss, New York, pp 253–355

    Google Scholar 

  • Hallas JM, Chichvarkhin A, Gosliner TM (2017) Aligning evidence: concerns regarding multiple sequence alignments in estimating the phylogeny of the Nudibranchia suborder Doridina. R Soc Open Sci 4(10):171095

    Article  Google Scholar 

  • Haszprunar G, Speimann E, Hawe A, Heß M (2011) Interactive 3D anatomy and affinities of the Hyalogyrinidae, basal Heterobranchia (Gastropoda) with a rhipidoglossate radula. Org Divers Evol 11(3):201–236

    Article  Google Scholar 

  • Hoffmann H (1939) Opisthobranchia. In: Dr. H.G. bronn’s klassen und ordnungen des tierreichs. Bd 3. Mollusca Abt 2,3,1 Gastropoda, 3 Buch. Akademische Verlagsgesellschaft, Leipzig, p xi+1247

  • Hughes RL (1979) Ultrastructure of the buccal mass in juvenile Coryphella salmonacea (Gastropoda: Nudibranchia). J Molluscan Stud 45(3):289–295

    Google Scholar 

  • Isarankura K, Runham NW (1968) Studies on the replacement of the gastropod radula. Malacologia 7(1):71–91

    Google Scholar 

  • Ivanov DL (1990) Proiskhozhdenie i rannie etapy evolutsionnykh preobrazovanij radulyarnogo apparata. In: Shileiko AA (ed) Evolutsionnaya morpholofiya molluskov (Zakonomernosti morfofunktsionalnykh perestroek radulyarnogo apparata). MSU Publ, Moscow, pp 5–37

    Google Scholar 

  • Kerth K (1973) Radulaersatz und Zellproliferation in der röntgenbestrahlten Radulascheide der Nacktschnecke Limax flavus L. Ergebnisse zur Arbeitsteilung der Scheidengewebe. Wilhelm Roux’ Archiv für Entwicklungsmechanik der Organismen 172(4):317–348

    Article  Google Scholar 

  • Kerth K (1979) Electron microscopic studies on radular tooth formation in the snails Helix pomatia L. and Limax flavus L. (Pulmonata, Stylommatophora). Cell Tissue Res 203(2):283–289

    Article  CAS  Google Scholar 

  • Kerth K (1983) Radulaapparat und Radulabildung der Mollusken II: Zahnbildung Abbau und Radulawachstum. Zoologische Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere 110(2):239–269

    Google Scholar 

  • Kerth K, Hänsch D (1977) Zellmuster und Wachstum des Odontoblastengürtels der Weinbergschnecke Helix pomatia L. Zoologische Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere 98(5):14–28

    Google Scholar 

  • Kerth K, Krause G (1969) Untersuchungen mittels Röntgenbestrahlung über den Radula-Ersatz der Nacktschnecke Limax flavus L. Wilhelm Roux Arch Entwickl Mech Org 164(1):48–82

    Article  Google Scholar 

  • Kohnert P, Brenzinger B, Jensen KR, Schrödl M (2013) 3D-microanatomy of the semiterrestrial slug Gascoignella aprica Jensen, 1985—a basal plakobranchacean sacoglossan (Gastropoda, Panpulmonata). Org Divers Evol 13(4):583–603

    Article  Google Scholar 

  • Korshunova T, Fletcher K, Picton B, Lundin K, Kashio S, Sanamyan N, Sanamyan K, Padula V, Schrödl M, Martynov A (2020) The Emperor’s Cadlina, hidden diversity and gill cavity evolution: new insights for the taxonomy and phylogeny of dorid nudibranchs (Mollusca: Gastropoda). Zool J Linn Soc 189(3):762–827

    Article  Google Scholar 

  • Lutfy RG, Demian ES (1967) The histology of the alimentary system of Marisa cornuarietis (Mesogastropoda: Ampullariidae). Malacologia 5(3):375–422

    Google Scholar 

  • Mackenstedt U, Märkel K (1987) Experimental and comparative morphology of radula renewal in pulmonates (Mollusca, Gastropoda). Zoomorphology 107(4):209–239

    Article  Google Scholar 

  • Mackenstedt U, Märkel K (2001) Radular structure and function. In: Barker GM (ed) The biology of terrestrial molluscs. CABI Publishing, New York, pp 213–236

    Chapter  Google Scholar 

  • Messenger JB, Young JZ (1999) The radular apparatus of cephalopods. Phil Trans R Soc London B Bio Sci 354(1380):161–182

    Article  Google Scholar 

  • Mikhlina A, Tzetlin A, Vortsepneva E (2018) Renewal mechanisms of buccal armature in Flabellina verrucosa (Nudibranchia: Aeolidida: Flabellinidae). Zoomorphology 137(1):31–50

    Article  Google Scholar 

  • Miller MC (1996) A new species of the dorid nudibranch genus Polycera Cuvier, 1816 (Gastropoda: Opisthobranchia) from New Zealand. J Molluscan Stud 62(4):443–450

    Article  Google Scholar 

  • Miller MC (2001) Descriptions of the dorid nudibranchs Polycera hedgpethi Marcus, 1964 and P. fujitai Baba, 1937 in New Zealand (Gastropoda: Opisthobranchia.) J Molluscan Stud 67(4):491–499

  • Millonig G (1964) Study on the factors which influence preservation of fine structure. In: Symposium on electron microscopy. Rome: Consiglio Nazionale delle Ricerche, Rome, p 347

  • Mischor B, Märkel K (1984) Histology and regeneration of the radula of Pomacea bridgesi (Gastropoda, Prosobranchia). Zoomorphology 104(1):42–66

    Article  Google Scholar 

  • Morton JE (1955) The functional morphology of Otina otis, a primitive marine pulmonate. J Mar Biol Assoc UK 34(1):113–150

    Article  Google Scholar 

  • Nybakken J, McDonald G (1981) Feeding mechanisms of West American nudibranchs feeding on Bryozoa, Cnidaria and Ascidiacea, with special respect to the radula. Malacologia 20(2):439–449

    Google Scholar 

  • Paz-Sedano S, Martín Álvarez JF, Gosliner TM, Pola M (2022) Reassessing North Eastern Atlantic-Mediterranean species of Trapania (Mollusca, Nudibranchia). Zoolog Scr 51(4):447–459

    Article  Google Scholar 

  • Peters W (1979) Basal bodies in the odontoblasts of the limpet, Patella coerulea L.(Gastropoda). Cell Tissue Res 202(2):295–301

    Article  CAS  Google Scholar 

  • Ponder WF, Lindberg DR, Ponder JM (2019) Biology and evolution of the mollusca, vol 1. CRC Press, Boca Raton, p 924

    Book  Google Scholar 

  • Rinkevich B (1993) Major primary stages of biomineralization in radular teeth of the limpet Lottia gigantea. Mar Biol 117(2):269–277

    Article  Google Scholar 

  • Rudman WB (1971) Structure and functioning of the gut in the Bullomorpha (Opisthobranchia) Part 1 Herbivores. J Natural His 5(6):647–675

    Article  Google Scholar 

  • Rudman WB (1982) The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: Chromodoris quadricolor, C. lineolata and Hypselodoris nigrolineata colour groups. Zoo J Linnean Soc 76(3):183–241

    Article  Google Scholar 

  • Rudman WB (1985) The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: Chromodoris aureomarginata, C. verrieri and C. fidelis colour groups. Zoological Journal of the Linnean Society 83(3):241–299

    Article  Google Scholar 

  • Rudman WB (1987) The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: Chromodoris epicuria, C. aureopurpurea, C. annulata, C. coi and Risbecia tryoni colour groups. Zoo J Linnean Soc 90(4):305–407

    Article  Google Scholar 

  • Rudman WB (1990) The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: further species of Glossodoris, Thorunna and the Chromodoris aureomarginata colour group. Zool J Linn Soc 100(3):263–326

    Article  Google Scholar 

  • Ruthensteiner B (2008) Soft Part 3D visualization by serial sectioning and computer reconstruction. Zoosymposia 1:63–100

    Article  Google Scholar 

  • Ruthensteiner B, Heß M (2008) Embedding 3D models of biological specimens in PDF publications. Microsc Res Tech 71(11):778–786

    Article  Google Scholar 

  • Sasaki T (1998) Comparative anatomy and phylogeny of the recent Archaeogastropoda (Mollusca: Gastropoda). Univer Museum UniverTok Bulletin 38:1–223

    Google Scholar 

  • Sørensen CG, Rauch C, Pola M, Malaquias MAE (2020) Integrative taxonomy reveals a cryptic species of the nudibranch genus Polycera (Polyceridae) in European waters. J Mar Biol Assoc UK 100(5):733–752

    Article  Google Scholar 

  • Valdés À (2002) A phylogenetic analysis and systematic revision of the cryptobranch dorids (Mollusca, Nudibranchia, Anthobranchia). Zool J Linn Soc 136(4):535–636

    Article  Google Scholar 

  • Valdés À, Gosliner TM (1999) Phylogeny of the radula-less dorids (Mollusca, Nudibranchia), with the description of a new genus and a new family. Zoolog Scr 28(3–4):315–360

    Article  Google Scholar 

  • von Salvini-Plawen L, 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 

  • Vortsepneva E (2020) Radula morphology of Clione limacina (Phipps, 1774)(Gastropoda: Heterobranchia: Gymnosomata). Invertebrate Zoo 17(3):291–309

    Article  Google 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. Zoologichesky Zhurnal 93:466–478

    Google Scholar 

  • Vortsepneva E, Tzetlin A (2019) General morphology and ultrastructure of the radula of Testudinalia testudinalis (OF Müller, 1776) (Patellogastropoda Gastropoda). J Morphology 280(11):1714–1733

    Article  Google Scholar 

  • 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(4):359–377

    Article  Google Scholar 

  • Vortsepneva E, Ivanov D, Purschke G, Tzetlin A (2014) Fine morphology of the jaw apparatus of Puncturella noachina (Fissurellidae, Vetigastropoda). J Morphol 275(7):775–787

    Article  Google Scholar 

  • Vortsepneva E, Tzetlin AB, Kantor Y (2019) First ultrastructural study of the formation of the hypodermic radula teeth of Conus (Neogastropoda: Conidae). J Molluscan Stud 85(2):184–196

    Article  Google Scholar 

  • Vortsepneva E, Herbert DG, Kantor Y (2020) Radula formation in two species of Conoidea (Gastropoda). J Morphol 281(10):1328–1350

    Article  CAS  Google Scholar 

  • Vortsepneva E, Herbert DG, Kantor Y (2021a) The rhipidoglossan radula: Formation and development in Margarites helicinus Phipps, 1774 (Trochoidea, Vetigastropoda). J Morphol 282(11):1683–1697

    Article  Google Scholar 

  • Vortsepneva E, Herbert DG, Kantor Y (2021b) The rhipidoglossan radula: formation and morphology of the radula in Puncturella noachina (Linnaeus, 1771)(Fissurellidae, Vetigastropoda). J Morphol 282(10):1523–1532

    Article  Google Scholar 

  • Vortsepneva E, Herbert DG, Kantor Y (2022) The rhipidoglossan radula: radular morphology and formation in Nerita litterata Gmelin, 1791 (Neritimorpha, Neritidae). J Morphol 283(3):363–373

    Article  Google Scholar 

  • Wägele H, Willan RC (2000) Phylogeny of the Nudibranchia. Zool J Linn Soc 130(1):83–181

    Article  Google Scholar 

  • Wägele H, Klussmann-Kolb A, Verbeek E, Schrödl M (2014) Flashback and foreshadowing—a review of the taxon Opisthobranchia. Org Divers Evol 14(1):133–149

    Article  Google Scholar 

  • Wiesel R, Peters W (1978) Licht- und elektronenmikroskopische Untersuchungen am Radulakomplex und zur Radulabildung von Biomphalaria glabrata Say (= Australorbis gl.) (Gastropoda, Basommatophora). Zoomorphologie 89(1):73–92

    Article  Google Scholar 

  • Wollscheid-Lengeling E, Boore J, Brown W, Wägele H (2001) The phylogeny of Nudibranchia (Opisthobranchia, Gastropoda, Mollusca) reconstructed by three molecular markers. Org Divers Evol 1(4):241–256

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank the divers’ team of the N.A. Pertsov White Sea Biological Station for help with providing material. Additionally, we are grateful to Fyodor Plandin (Lomonosov Moscow State University) for help with micro-CT. The electron microscopy investigations were performed at the User Facilities Centre of Lomonosov Moscow State University, at the Centre of microscopy WSBS MSU and at the Institute for Biology of Inland Waters of the Russian Academy of Sciences. Dr. Bernhard Ruthensteiner (ZSM) and an anonymous reviewer are thanked for their valuable comments, which helped to improve the manuscript. This study was conducted in frame of scientific projects of the State Order of the Russian Federation Government to Lomonosov Moscow State University No. 121032500077-8 and No. 121032300121-0 with financial support of Russian Science Foundation, Grant No. 21-14-00042.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: EV; Light microscopy studies: EV, AM; 3D reconstruction: AM; Scanning electron microscopy studies: EV, AM; Transmission electron microscopy studies: EV; Micro-CT studies: EL; Writing-original draft preparation: AM, EV; Writing – review and editing: AM, EL, EV; Supervising: EV.

Corresponding author

Correspondence to A. Mikhlina.

Ethics declarations

Competing interests

The authors declare no competing interests.

Conflict of interest

The authors have no conflicts of interests to declare that are relevant to the content of this article.

Ethical approval

No approval of research ethics committees was required to accomplish the goals of this study because experimental work was conducted with an unregulated invertebrate species.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised: Errors in the figure references under the ‘Results’ section corrected to Figure 9a instead of Figure 8a.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 31420 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mikhlina, A., Lisova, E. & Vortsepneva, E. Formation of buccal armature of Cadlina laevis (Linnaeus, 1767) (Nudibranchia, Gastropoda). Zoomorphology 141, 245–261 (2022). https://doi.org/10.1007/s00435-022-00576-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-022-00576-2

Keywords

Navigation