Skip to main content
SpringerLink
Log in

3D-microanatomy and histology of the hydrothermal vent gastropod Lurifax vitreus Warén & Bouchet, 2001 (Heterobranchia: Orbitestellidae) and comparisons with Ectobranchia

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

Up to now, the internal anatomy of representatives of only two of three recent genera of the Orbitestellidae have been described. Herein, a species of the third genus, Lurifax vitreus from hydrothermal vent sites of the North Atlantic, is examined on the basis of semi-thin sections. Data on three-dimensional (3D)-anatomy and histology are provided in order to increase knowledge of the family. In addition, the original serial sections of Orbitestella wareni and Microdiscula cf. subcanaliculata of the original paper by Ponder (Journal of Molluscan Studies 56:515–532, 1990a) were reinvestigated and compared with Lurifax vitreus. Although Lurifax vitreus is significantly larger than the two former genera, it is again devoid of a gill but shows opponent ciliary stripes and a pallial tentacle. Most orbitestellid characters reflect plesiomorphic conditions among the Heterobranchia; autapomorphies of the family include an orthostrophic protoconch, massive jaws, a diagnostic radula type, paired posterior pedal glands with a common opening, and a pedally innervated copulatory organ. In agreement with actual molecular trees, our data suggest a placement of Orbitestellidae as basic Heterobranchia outside of Ectobranchia (Valvatoidea).

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bäumler, N., Haszprunar, G., & Ruthensteiner, B. (2008). 3D interactive microanatomy of Omalogyra atomus (Philippi, 1841) (Gastropoda, Heterobranchia, Omalogyridae). In D. Geiger, & B. Ruthensteiner (Eds.) Micromolluscs: methodological challenges—exciting results. Zoosymposia, 1:108–116.

  • Bernard, F. (1890). Recherches sur Valvata piscinalis. Bulletin Scientifique de la France Belgique, 22, 253–361. pls. 12–20.

    Google Scholar 

  • Bieler, R. (1992). Gastropod phylogeny and systematics. Annual Review of Ecology and Systematics, 23, 311–338.

    Article  Google Scholar 

  • Bieler, R., Ball, A. D., & Mikkelsen, P. M. (1998). Marine Valvatoidea—comments on anatomy and systematics with description of a new species from Florida (Heterobranchia: Cornirostridae). Malacologia, 40, 305–320.

    Google Scholar 

  • Bosch, D. T., Dance, S. P., Moolenbeek, R., & Oliver, P. G. (1995). Seashells of Eastern Arabia. Dubai: Motivate.

    Google Scholar 

  • Brenzinger, B., Wilson, N. G., & Schrödl, M. (2011). 3D microanatomy of a gastropod ´worm´, Rhodope rousei n.sp. (Heterobranchia) from Southern Australia. Journal of Molluscan Studies, 77, 375–387.

    Article  Google Scholar 

  • Brenzinger, B., Haszprunar, G., & Schrödl, M. (2013a). At the limits of a successful body plan – 3D microanatomy, histology and evolution of Helminthope (Mollusca: Heterobranchia: Rhodopemorpha), the most worm-like gastropod. Frontiers in Zoology, 10, 37.

    Article  PubMed Central  PubMed  Google Scholar 

  • Brenzinger, B., Wilson, N. G., & Schrödl, M. (2013). A glimpse into early heterobranch evolution—microanatomy of Murchisonellidae. In: Abstracts of the 18th WCM, Ponta Delgada, Azores (A. M. de Frias Martins, A. C. Costa, R. T. da Cunha, S. Ávila, S. C. Monteiro & P. Raposeiro, eds.). Açoreana Supplemento, 8: 180–181.

  • Bush, K. J. (1897). Revision of the marine gastropods referred to Cyclostrema, Adeorbis, Vitrinella, and related genera: with descriptions of some new genera and species belonging to the Atlantic fauna of America. Transactions of the Connecticut Academy of Arts and Sciences, 10, 97–144. pls. 22, 23.

    Google Scholar 

  • Chia, F.-S., Koss, R., & Bickell, L. R. (1981). Fine structural study of the statocysts in the veliger larva of the nudibranch Rostanga pulchra. Cell and Tissue Research, 214, 67–80.

    Article  CAS  PubMed  Google Scholar 

  • Cleland, D. M. (1954). A study of the habits of Valvata piscinalis (Müller) and the structure and function of the alimentary canal and reproductive system. Journal of Molluscan Studies, 30, 167–203.

    Google Scholar 

  • Cuvelier, A., Sarradin, P. M., Sarrazin, J., Colaço, A., Copley, J. T., Desbruyères, D., Glover, A. G., Santos, R. S., & Tyler, P. (2011). Hydrothermal faunal assemblages and habitat characterisation at the Eiffel Tower edifice (Lucky Strike, Mid-Atlantic Ridge). Marine Ecology, 32, 243–255.

    Article  Google Scholar 

  • Dinapoli, A., & Klussmann-Kolb, A. (2010). The long way to diversity—phylogeny and evolution of the Heterobranchia (Mollusca: Gastropoda). Molecular Phylogenetics and Evolution, 55, 60–76.

    Article  PubMed  Google Scholar 

  • Dinapoli, A., Zinssmeister, C., & Klussmann-Kolb, A. (2011). New insights into the phylogeny of the Pyramidellidae (Gastropoda). Journal of Molluscan Studies, 77, 1–7.

    Article  Google Scholar 

  • Fretter, V. (1948). The structure and life history of some minute prosobranchs of rock pools: Skeneopsis planorbis (Fabricius), Omalogyra atomus (Philippi), Rissoella diaphana (Alder) and Rissoella opalina (Jeffreys). Journal of the Marine Biological Association of the United Kingdom, 27, 597–632.

    Article  Google Scholar 

  • Fretter, V., & Graham, A. (1954). Observations on the opisthobranch mollusc Acteon tornatilis (L.). Journal of the Marine Biological Association of the United Kingdom, 33, 565–585.

    Article  Google Scholar 

  • Gatliff, J. H. (1906). On some Victorian marine Mollusca, new species, and others little known. Proceedings of the Royal Society of Victoria, N.S, 19, 1–4. pls. 1–2.

    Google Scholar 

  • Giuste, F., & Sbrana, C. (2012). Lurifax vitreus Warén & Bouchet, 2001 (Gastropoda, Orbitestellidae), a new record for deep waters of the Tuscan Archipelago (Tyrrhenian Sea, Italy). Biodiversity Journal, 3, 91–92.

    Google Scholar 

  • Göbbeler, K., & Klussmann-Kolb, A. (2011). Molecular phylogeny of the Euthyneura (Mollusca, Gastropoda) with special focus on Opisthobranchia as a framework for reconstruction of evolution of diet. Thalassas, 27, 121–154.

    Google Scholar 

  • Handschuh, S., Schwaha, T., & Metscher, B. D. (2010). Showing their true colors: a practical approach to volume rendering from serial sections. BMC Development Biology, 10(41), 16.

    Google Scholar 

  • Haszprunar, G. (1985a). The Heterobranchia—a new concept of the phylogeny of the higher Gastropoda. Journal of Zoological Systematics and Evolutionary Research, 23, 15–37.

    Article  Google Scholar 

  • Haszprunar, G. (1985b). Zur Anatomie und systematischen Stellung der Architectonicidae (Mollusca, Allogastropoda). Zoologica Scripta, 14, 25–43.

    Article  Google Scholar 

  • Haszprunar, G. (1985c). On the anatomy and systematic position of the Mathildidae (Mollusca, Allogastropoda). Zoologica Scripta, 14, 201–213.

    Article  Google Scholar 

  • Haszprunar, G. (1987). The fine structure of the ctenidial sense organs (bursicles) of Vetigastropoda (Zeugobranchia, Trochoidea) and their functional and phylogenetic significance. Journal of Molluscan Studies, 53, 46–51.

    Google Scholar 

  • Haszprunar, G. (1988). On the origin and evolution of major gastropod groups, with special reference to the Streptoneura. Journal of Molluscan Studies, 54, 367–441.

    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. Organisms, Diversity and Evolution, 11, 201–236.

    Article  Google Scholar 

  • Hawe, A., Heß, M., & Haszprunar, G. (2013a). 3D-reconstruction of the anatomy of the ovoviviparous (?) freshwater gastropod Borysthenia naticina (Menke, 1845) (Ectobranchia: Valvatidae). Journal of Molluscan Studies, 79, 191–204.

    Article  Google Scholar 

  • Hawe, A., Gensler, H., & Haszprunar, G. (2013b). Endosymbiotic bacteria in the hot-vent gastropod Lurifax vitreus (Heterobranchia: Orbitestellidae). In: Abstracts of the 18th WCM, Ponta Delgada, Azores (A. M. de Frias Martins, A. C. Costa, R. T. da Cunha, S. Ávila, S. C. Monteiro & P. Raposeiro, eds.). Açoreana Supplemento, 8: 76.

  • Healy, J. M. (1990). Spermatozoa and spermiogenesis of Cornirostra, Valvata and Orbitestella (Gastropoda: Heterobranchia) with a discussion of valvatoidean sperm morphology. Journal of Molluscan Studies, 56, 557–566.

    Article  Google Scholar 

  • Healy, J. M. (1991). Sperm morphology in the marine gastropod Architectonica perspectiva (Mollusca): unique features and systematic relevance. Marine Biology, 109, 59–65.

    Google Scholar 

  • Healy, J. M. (1993). Comparative sperm ultrastructure and spermiogenesis in basal heterobranch gastropods (Valvatoidea, Architectonicoidea, Rissoelloidea, Omalogyroidea, Pyramidelloidea) (Mollusca). Zoologica Scripta, 22, 263–276.

    Article  Google Scholar 

  • Heß, M., Beck, F., Gensler, H., Kano, Y., Kiel, S., & Haszprunar, G. (2008). Microanatomy, shell structure and molecular phylogeny of Leptogyra, Xyleptogyra and Leptogyropsis (Gastropoda: Neomphalida: Melanodrymiidae) from sunken wood. Journal of Molluscan Studies, 74, 383–401.

    Article  Google Scholar 

  • Høisaeter, T., & Johannessen, P. J. (2002). Xylodiscula planata sp. nov., a “lower” heterobranch gastropod from Norwegian waters. Sarsia, 86, 325–332.

    Google Scholar 

  • Huber, G. (1993). On the cerebral nervous system of marine Heterobranchia (Gastropoda). Journal of Molluscan Studies, 59, 381–420.

    Article  Google Scholar 

  • Iredale, T. (1917). More molluscan name-changes, generic and specific. Proceedings of the Malacological Society of London, 12, 322–330.

    Google Scholar 

  • Jablonski, D., & Lutz, R. A. (1983). Larval ecology of marine benthic invertebrates: paleobiological implications. Biological Reviews, 58, 21–89.

    Article  Google Scholar 

  • Jörger, K. M., Stöger, I., Kano, Y., Fukuda, H., Knebelsberger, T., & Schrödl, M. (2010). On the origin of Acochlidia and other enigmatic euthyneuran gastropods, with implications for the systematics of Heterobranchia. BMC Evolutionary Biology, 10(323), 20.

    Google Scholar 

  • Kiel, S. (2006). New records and species of molluscs from tertiary cold-seep carbonates in Washington State, USA. Journal of Paleontology, 80, 121–137.

    Article  Google Scholar 

  • Lartaud, F., Little, C. T. S., de Rafelis, M., Bayon, G., Dyment, J., Ildefonse, B., Gressier, V., Fouquet, Y., Gaill, F., & Le Bris, N. (2011). Fossil evidence for serpentinization fluids fueling chemosynthetic assemblages. Proceedings of the National Academy of Sciences of the United States of America, 108(19), 7698–7703.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lima, S. F. B., de Barros, J. C. N., Francisco, J. A., & Oliveira, P. S. (2011). New records of Caribbean Gastropods (Skeneidae, Tornidae, Orbitestellidae and Omalogyridae) for Saint Peter and Saint Paul Archipelago (Brazil). Tropical Zoology, 24, 87–106.

    Google Scholar 

  • Marshall, B. A. (1988). Skeneidae, Vitrinellidae and Orbitestellidae (Mollusca, Gastropoda) associated with biogenic substrata from bythal depth off New Zealand and New South Wales. Journal of Natural History, 22, 969–1004.

    Article  Google Scholar 

  • Moolenbeek, R. G. (1994). The Orbitestellidae (Gastropoda: Heterobranchia) of the Sultanate of Oman with description of a new genus and two new species. Apex, 9, 5–10.

    Google Scholar 

  • Nützel, A., Lehnert, O., & Fryda, J. (2006). Origin of planktotrophy—evidence from early molluscs. Evolution & Development, 8, 325–330.

    Article  Google Scholar 

  • Pilsbry, H. A., & Olsson, A. A. (1945). Vitrinellidae and similar gastropods of the Panamic Province. Part I. Proceedings of the Academy of Natural Sciences of Philadelphia, 97, 249–278.

    Google Scholar 

  • Ponder, W. F. (1967). The classification of the Rissoidae and Orbitestellidae with descriptions of some new taxa. Transactions of the Royal Society of New Zealand, Zoology, 9(17), 193–244.

    Google Scholar 

  • Ponder, W. F. (1990a). The anatomy and relationships of the Orbitestellidae (Gastropoda: Heterobranchia). Journal of Molluscan Studies, 56, 515–532.

    Article  Google Scholar 

  • Ponder, W. F. (1990b). The anatomy and relationships of a marine valvatoidean (Gastropoda: Heterobranchia). Journal of Molluscan Studies, 56, 533–555.

    Article  Google Scholar 

  • Ponder, W. F. (1991). Marine valvatoidean gastropods—implications for early heterobranch phylogeny. Journal of Molluscan Studies, 57, 21–32.

    Article  Google Scholar 

  • Ponder, W. F., & de Keyser, R. G. (1998). Superorder Valvatoidea. In P. L. Beesley, G. J. B. Ross, & A. Wells (Eds.), Mollusca: The Southern Synthesis. Fauna of Australia Vol. 5B (pp. 854–858). Melbourne: CSIRO Publishing.

    Google Scholar 

  • Ponder, W. F., & Lindberg, D. R. (1997). Towards a phylogeny of gastropod molluscs: an analysis using morphological characters. Zoological Journal of the Linnean Society, 119, 83–265.

    Google Scholar 

  • Ponder, W. F., & Yoo, E. K. (1977). A revision of the Australian species of the Rissoellidae (Mollusca: Gastropoda). Records of the Australian Museum, 31, 133–185.

    Article  Google Scholar 

  • Rath, E. (1986). Beiträge zur Anatomie und Ontogenie der Valvatidae (Mollusca: Gastropoda). PhD-Thesis, Faculty of Biology, University of Vienna, Vienna, 263 pp.

  • Rath, E. (1988). Organization and systematic position of the Valvatidae. Malacological Review, Supplement, 4, 194–204.

    Google Scholar 

  • Richardson, K. C., Jarett, L., & Finke, E. H. (1960). Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Biotechnic & Histochemistry, 35, 313–323.

    Article  CAS  Google Scholar 

  • Robertson, R. (1985). Four characters and the higher category systematics of gastropods. American Malacological Bulletin Special Edition, 1, 1–22.

    Google Scholar 

  • Robertson, R. (2012). Pyramidellid protoconchs, eggs, embryos and larval ecology: an introductory survey. American Malacological Bulletin, 30, 219–228.

    Article  Google Scholar 

  • Rodriguez-Babio, C. E. (1982). Sobre la morfologia de las protoconchas y el dessarrollo larvario de algunas especies de gasteropodos prosobranquios de la region de Roscoff. Trabajos Compostelanos de Biología, 9, 31–48.

    Google Scholar 

  • Rodriguez-Babio, C. E., & Rubio, F. (1993). Contribución al conocimiento de Tjaernoeia unisulcata (Chaster, 1896) (Gastropoda, Heterobranchia, Tjaernoeidae). Iberus, 11, 75–77.

    Google Scholar 

  • Rodriguez-Babio, C. E., & Thiriot-Quievreux, C. (1974). Gastéropodes de la region de Roscoff. Etude particulaire de la protoconque. Cahiers de Biologie Marine, 15, 531–549.

    Google Scholar 

  • Roy, K. O.-L., Sibuet, M., Fiala-Médioni, A., Gofas, S., Salas, C., Mariotti, A., et al. (2004). Cold seep communities in the deep eastern Mediterranean Sea: composition, symbiosis and spatial distribution on mud volcanoes. Deep-Sea Research Part I, 51, 1915–1936.

    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. Microscopy Research and Technique, 71, 778–786.

    Article  PubMed  Google Scholar 

  • Ruthensteiner, B., Bäumler, N., & Barnes, D. G. (2010). Interactive 3D volume rendering in biomedical publications. Micron, 41, 886–898.

    Article  PubMed  Google Scholar 

  • Salvini-Plawén, L. V. & Haszprunar, G. (1987). The Vetigastropoda and the systematics of streptoneurous Gastropoda (Mollusca). Journal of Zoology, 211, 747–770.

    Google Scholar 

  • Sasaki, T., & Okutani, T. (2005). A new species of Lurifax (Gastropoda: Heterobranchia: Orbitestellidae) from Sumisu Caldera, Southern Japan. Venus, Japanese Journal of Malacology, 63, 121–124.

    Google Scholar 

  • Schrödl, M., Jörger, K. M., Klussmann-Kolb, A., & Wilson, N. G. (2011). Bye Bye "Opisthobranchia"! A review on the contribution of mesopsammic sea slugs to euthyneuran systematics. Thalassas, 27, 101–112.

    Google Scholar 

  • Simone, L. R. L., & Zelaya, D. G. (2004). A new Orbitestella (Gastropoda: Heterobranchia: Orbitestellidae) from Tierra del Fuego, Argentina. The Nautilus, 118, 160–166.

    Google Scholar 

  • Smriglio, C., & Mariottini, P. (2002). Lurifax vitreus Warén & Bouchet, 2001 (Gastropoda, Orbitestellidae), first report from Western Mediterranean Sea. Bolletino di Malacologico (Milano), 38, 45–47.

    Google Scholar 

  • Strong, E. E. (2003). Refining molluscan characters: morphology, character coding and a phylogeny of the Caenogastropoda. Zoological Journal of the Linnean Society, 137, 447–554.

    Article  Google Scholar 

  • Warén, A. (1991). New and little known Mollusca from Iceland and Scandinavia. Sarsia, 76, 53–124.

    Google Scholar 

  • Warén, A. (1992). New and little known „skeneiomorph“ gastropods from the Mediterranean Sea and the adjacent atlantic ocean. Bolletino di Malacologico (Milano), 27, 149–248.

    Google Scholar 

  • Warén, A. (2013). Murchisonellidae: who they are, where are they and what are they doing? (Gastropoda, lowermost Heterobranchia). Vita Malacologia, 11, 1–14.

    Google Scholar 

  • Warén, A., & Bouchet, P. (2001). Gastropoda and Monoplacophora from hydrothermal vents and seeps; new taxa and records. Zoologica Scripta, 44, 116–231.

    Google Scholar 

  • Wiederhold, M. L., Sharma, J. S., Driscoll, B. P., & Harrison, J. L. (1990). Development of the statocyst in Aplysia californica. I. Observations on statoconial development. Hearing Research, 49, 63–78.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, N. G., Jörger, K. M., & Schrödl, M. (2010). Reducing an enigma: placing the vermiform Rhodopemorpha (Gastropoda) in a phylogeny [abstract]. Tropical Natural History, 3, 37.

    Google Scholar 

Download references

Acknowledgments

We are deeply indebted to Anders Warén (Swedish Museum of Natural History, Stockholm) for sending us the specimens of Lurifax vitreus and to Winston F. Ponder (Australian Museum Sydney), who sent us his original sections of Orbitestella and Microdiscula and gave helpful comments on the typescript. Martin Heß (LMU) provided significant help to compiling the interactive pdf. We also thank Katharina Jörger (LMU), two anonymous reviewer and the editor for helpful comments on the typescript and the illustrations. The Bayerische Eliteförderung provided a PhD-fellowship for A.H.

Author information

Authors and Affiliations

  1. Department Biology II, Ludwig-Maximilians-Universität München, BioZentrum, Großhaderner Str. 2, 82152, Planegg, Germany

    Andreas Hawe & Gerhard Haszprunar

  2. Zoologische Staatssammlung München, Münchhausenstraße 21, 81247, München, Germany

    Gerhard Haszprunar

  3. GeoBio-Center, Ludwig-Maximilians-Universität München, Planegg, Germany

    Gerhard Haszprunar

Authors
  1. Andreas Hawe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gerhard Haszprunar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andreas Hawe.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure 1

(PDF 5.58 mb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hawe, A., Haszprunar, G. 3D-microanatomy and histology of the hydrothermal vent gastropod Lurifax vitreus Warén & Bouchet, 2001 (Heterobranchia: Orbitestellidae) and comparisons with Ectobranchia. Org Divers Evol 14, 43–55 (2014). https://doi.org/10.1007/s13127-013-0155-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-013-0155-1

Keywords

Search

Navigation