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

Zoomorphologie - Tập 141 - Trang 245-261 - 2022
A. Mikhlina1, E. Lisova1, E. Vortsepneva1
1Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia

Tóm tắt

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.

Tài liệu tham khảo

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 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 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 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 Dennis MM, Molnár K, Kriska G, Lőw P (2021) Mollusca: Gastropoda. In: LaDouceur EEB (ed) Invertebrate histology. Wiley-Blackwell, Hoboken, NJ, pp 87–132 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 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 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 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 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 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 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 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 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 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 Isarankura K, Runham NW (1968) Studies on the replacement of the gastropod radula. Malacologia 7(1):71–91 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 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 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 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 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 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 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 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 Lutfy RG, Demian ES (1967) The histology of the alimentary system of Marisa cornuarietis (Mesogastropoda: Ampullariidae). Malacologia 5(3):375–422 Mackenstedt U, Märkel K (1987) Experimental and comparative morphology of radula renewal in pulmonates (Mollusca, Gastropoda). Zoomorphology 107(4):209–239 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 Messenger JB, Young JZ (1999) The radular apparatus of cephalopods. Phil Trans R Soc London B Bio Sci 354(1380):161–182 Mikhlina A, Tzetlin A, Vortsepneva E (2018) Renewal mechanisms of buccal armature in Flabellina verrucosa (Nudibranchia: Aeolidida: Flabellinidae). Zoomorphology 137(1):31–50 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 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 Morton JE (1955) The functional morphology of Otina otis, a primitive marine pulmonate. J Mar Biol Assoc UK 34(1):113–150 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 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 Peters W (1979) Basal bodies in the odontoblasts of the limpet, Patella coerulea L.(Gastropoda). Cell Tissue Res 202(2):295–301 Ponder WF, Lindberg DR, Ponder JM (2019) Biology and evolution of the mollusca, vol 1. CRC Press, Boca Raton, p 924 Rinkevich B (1993) Major primary stages of biomineralization in radular teeth of the limpet Lottia gigantea. Mar Biol 117(2):269–277 Rudman WB (1971) Structure and functioning of the gut in the Bullomorpha (Opisthobranchia) Part 1 Herbivores. J Natural His 5(6):647–675 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 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 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 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 Ruthensteiner B (2008) Soft Part 3D visualization by serial sectioning and computer reconstruction. Zoosymposia 1:63–100 Ruthensteiner B, Heß M (2008) Embedding 3D models of biological specimens in PDF publications. Microsc Res Tech 71(11):778–786 Sasaki T (1998) Comparative anatomy and phylogeny of the recent Archaeogastropoda (Mollusca: Gastropoda). Univer Museum UniverTok Bulletin 38:1–223 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 Valdés À (2002) A phylogenetic analysis and systematic revision of the cryptobranch dorids (Mollusca, Nudibranchia, Anthobranchia). Zool J Linn Soc 136(4):535–636 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 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 Vortsepneva E (2020) Radula morphology of Clione limacina (Phipps, 1774)(Gastropoda: Heterobranchia: Gymnosomata). Invertebrate Zoo 17(3):291–309 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 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 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 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 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 Vortsepneva E, Herbert DG, Kantor Y (2020) Radula formation in two species of Conoidea (Gastropoda). J Morphol 281(10):1328–1350 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 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 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 Wägele H, Willan RC (2000) Phylogeny of the Nudibranchia. Zool J Linn Soc 130(1):83–181 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 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 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