Skip to main content
SpringerLink
Log in

Insemination by a kiss? Interactive 3D-microanatomy, biology and systematics of the mesopsammic cephalaspidean sea slug Pluscula cuica Marcus, 1953 from Brazil (Gastropoda: Euopisthobranchia: Philinoglossidae)

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

Abstract

Increasing molecular evidence suggests that the phylogeny of euthyneuran gastropods differs greatly from centenary textbook concepts. The presence, homology and evolution of characters in major subgroups thus need to be reinvestigated. Traditionally basal opisthobranch Cephalaspidea (“head-shield snails and slugs”) were pruned to a new taxon concept, with benthic euopisthobranch and tentacle-bearing cephalaspidean lineages basal to burrowing, head-shield bearing philinoidean species. Among the latter, mesopsammic “microslug” lineages evolved at least twice. Herein we explore in 3D microanatomical detail the putatively basal philinoglossan Pluscula cuica (Marcus, Boletim da Faculdade de Filosofia, Ciências e Letras. Universidade de São Paulo 164:165–203, 1953a) from its type locality in Brazil. The species possesses several “accessory” ganglia and a reduced posterior mantle cavity that retains some putative shell-building tissue and an osphradium. The hermaphroditic, monaulic genital system opens in a posterior position; it retains a bursa copulatrix but lacks a distinct receptaculum seminis. Autosperm is transferred to the cephalic copulatory organ via an external sperm groove, not through the hemocoel, as suggested in the original description. The penis opens through the oral tube, sperm is transferred by a “kiss”. A conspicuous yellow gland is discussed as a modified Blochmann’s gland. Retaining several putative symplesiomorphies with philinoids, Pluscula is discussed as the most basal offshoot in meiofaunal Philinoglossidae. However, the supposed “primitiveness” of the fused rather than separate cerebropleural ganglia and the triganglionate rather than pentaganglionate visceral nerve cord was based on misobservations. Higher categories such as Philinoglossacea for Philinoglossidae, and a separate family Plusculidae for P. cuica are no longer warranted. Inner cephalaspidean relationships and a scenario of more or less successive philinoglossid adaptation to meiofaunal environments should be investigated by molecular studies with more comprehensive taxon sampling.

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

  • Anthes, N., & Michiels, N. K. (2007a). Precopulatory stabbing, hypodermic injections and unilateral copulations in a hermaphroditic sea slug. Biology Letters, 3, 121–124.

    Article  PubMed  Google Scholar 

  • Anthes, N., & Michiels, N. K. (2007b). Reproductive morphology, mating behavior, and spawning ecology of cephalaspid sea slugs (Aglajidae and Gastropteridae). Invertebrate Biology, 126(4), 335–365.

    Article  Google Scholar 

  • Arnaud, P. M., Poizat, C. L., & Salvini-Plawen, Lv. (1986). Marine-interstitial Gastropoda (including one freshwater interstitial species). In L. Botoseanu (Ed.), Stygofauna Mundi. A Faunistic, Distributional, and Ecological Synthesis of the World Fauna inhabiting Subterranean Waters (including the Marine Interstitial) (pp. 153–165). Leiden: Brill-Backhuys.

    Google Scholar 

  • Baba, K. (1937). Contribution to the Knowledge of a Nudibranch, Okadaia elegans Baba. Japanese Journal of Zoology, 7, 147–190.

    Google Scholar 

  • Bartolomaeus, T. (1997). Ultrastructure of the renopericardial complex of the interstitial gastropod Philinoglossa helgolandica Hertling, 1935 (Mollusca: Opisthobranchia). Zoologischer Anzeiger, 235, 165–176.

    Google Scholar 

  • Beeman, R. (1977). Gastropoda: Opisthobranchia. In A. C. Giese & J. S. Pearse (Eds.), Reproduction of Marine Invertebrates (Vol. 4, pp. 115–179). New York: Academic.

    Chapter  Google Scholar 

  • Beesley, P. L., Ross, G. J. B., & Wells, A. (1998). Mollusca—The Southern Synthesis (Vol. 5B, p. 671). Melbourne: CSIRO.

    Google Scholar 

  • Bouchet, P., & Rocroi, J.-P. (2005). Classification and nomenclator of gastropod families. Malacologia, 47(1–2), 1–397.

    Google Scholar 

  • Brenzinger, B., Neusser, T. P., Jörger, K. M., & Schrödl, M. (2011a). Integrating 3D-microanatomy and molecules: natural history of the Pacific Acochlidian freshwater slug Strubellia Odhner, 1937, with description of a new species. Journal of Molluscan Studies, 77, 351–374.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Brodie, G. D., Klussmann-Kolb, A., & Gosliner, T. M. (2001). Anatomy and histology of a new species of Enotepteron (Cephalaspidea: Gastropteridae) from tropical northeastern Australia. Veliger, 44(4), 362–369.

    Google Scholar 

  • Brown, G. H. (1979). An investigation of the anatomy of Colpodaspis pusilla (Mollusca: Opisthobranchia) and a description of a new species of Colpodaspis from Tanzanian coastal waters. Journal of Zoology, London, 187, 201–221.

    Article  Google Scholar 

  • Burn, R., & Thompson, T. E. (1998). Superfamily Philinoidea. In P. L. Beesley, G. J. B. Ross, & A. Wells (Eds.), Mollusca: the Southern Synthesis. Fauna of Australia (Vol. 5B, pp. 948–954). Melbourne: CSIRO.

    Google Scholar 

  • Challis, D. A. (1968). A new genus and species of the order Acochlidiacea (Mollusca: Opisthobranchia) from Melanesia. Transactions of the Royal Society of New Zealand, 10(20), 191–197.

    Google Scholar 

  • Challis, D. A. (1969a). Philine exigua n. sp. (Opisthobranchia: Bullomorpha), a minute interstitial species from Melanesia. Transactions of the Royal Society of New Zealand, 11(12), 177–186.

    Google Scholar 

  • Challis, D. A. (1969b). Philinoglossa marcusi n.sp. (Mollusca: Opisthobranchia: Philinoglossacea) from the British Solomon Islands Protectorate. Transactions of the Royal Society of New Zealand, 11, 169–175.

    Google Scholar 

  • Cruz-Rivera, E. (2011). Evidence for chemical defence in the cephalaspidean Nakamigawaia spiralis Kuroda & Habe, 1961. Journal of Molluscan Studies, 77, 95–97.

    Article  Google Scholar 

  • Dayrat, B., & Tillier, S. (2000). Taxon sampling, character sampling and systematics: how gradist presuppositions created additional ganglia in gastropod euthyneuran taxa. Zoological Journal of the Linnean Society, 129, 403–418.

    Article  Google Scholar 

  • Dayrat, B., & Tillier, S. (2002). Evolutionary relationships of euthyneuran gastropods (Mollusca): a cladistic re-evaluation of morphological characters. Zoological Journal of the Linnean Society, 135, 403–470.

    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 

  • Eder, B., Schrödl, M., & Jörger, K. M. (2011). Systematics and redescription of the European meiofaunal slug Microhedyle glandulifera (Kowalevsky, 1901) (Heterobranchia: Acochlidia): evidence from molecules and morphology. Journal of Molluscan Studies, 77, 388–400.

    Article  Google Scholar 

  • Edlinger, K. (1980). Zur Phylogenie der chemischen Sinnesorgane einiger Cephalaspidea (Mollusca—Opisthobranchia). Zeitschrift für zoologische Systematik und Evolutionsforschung, 18, 241–256.

    Article  Google Scholar 

  • Faller, S., Staubach, S., & Klussmann-Kolb, A. (2008). Comparative immunohistochemistry of the cephalic sensory organs in Opisthobranchia (Mollusca, Gastropoda). Zoomorphology, 127, 227–239.

    Article  Google Scholar 

  • Franc, A. (1968). Opisthobranches. In P.-P. Grassé (Ed.), Traité de Zoologie. Anatomie, Systématique, Biologie. Vol. 5, Fasc. 3: Mollusques Gastéropodes et Scaphopodes (p. 612). Paris: Masson.

    Google Scholar 

  • Göbbeler, K., & Klussmann-Kolb, A. (2010). The phylogeny of the Acteonoidea (Gastropoda): Molecular systematics and first detailed morphological study of Rictaxis punctocaelatus (Carpenter, 1864). Journal of Molluscan Studies, 76(4), 303–316.

    Article  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(2), 121–154.

    Google Scholar 

  • Golding, R. E. (2010). Anatomy in Toledonia warenella n. sp. (Gastropoda: Opisthobranchia: Diaphanidae) visualized by three-dimensional reconstruction. Invertebrate Biology, 129, 151–164.

    Article  Google Scholar 

  • Gosliner, T. M. (1980). Systematics and phylogeny of the Aglajidae (Opisthobranchia: Mollusca). Zoological Journal of the Linnean Society, 68, 325–360.

    Article  Google Scholar 

  • Gosliner, T. M. (1989). Revision of the Gastropteridae (Opisthobranchia: Cephalaspidea) with descriptions of a new genus and six new species. Veliger, 32(4), 333–381.

    Google Scholar 

  • Gosliner, T. M. (1994). Gastropoda: Opisthobranchia. In F. W. Harrison & A. W. Kohn (Eds.), Microscopic Anatomy of Invertebrates, 5. Mollusca (pp. 253–355). New York: Wiley-Liss.

    Google Scholar 

  • Guiart, J. (1901). Contribution à l’étude des Gastéropodes Opisthobranches et en particulier des Céphalaspides. Mémoires de la Société Zoologique de France, 14, 1–219.

    Google Scholar 

  • Händeler, K., & Wägele, H. (2007). Preliminary study on molecular phylogeny of Sacoglossa and a compilation of their food organisms. Bonner zoologische Beiträge, 55(3/4), 231–254.

    Google Scholar 

  • Hanken, J., & Wake, D. B. (1993). Miniaturization of body size: organismal consequences and evolutionary significance. Annual Review of Ecology and Systematics, 24, 501–519.

    Article  Google Scholar 

  • Haszprunar, G. (1985). The Heterobranchia—a new concept of the phylogeny of the higher Gastropoda. Zeitschrift für zoologische Systematik und Evolutionsforschung, 23, 15–37.

    Article  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., & Huber, G. (1990). On the central nervous system of Smeagolidae and Rhodopidae, two families questionably allied with the Gymnomorpha (Gastropoda: Euthyneura). Journal of Zoology, London, 220, 185–199.

    Article  Google Scholar 

  • Hertling, H. (1932). Philinoglossa helgolandica, n. g., n. sp., ein neuer Opisthobranchier aus der Nordsee bei Helgoland. Wissenschaftliche Untersuchungen der Abteilung Helgoland, Neue Folge, 19, 1–9.

    Google Scholar 

  • Higgins, R. P., & Thiel, H. (1988). Introduction to the Study of Meiofauna. London/Washington D.C.: Smithsonian Institution Press.

    Google Scholar 

  • Horikoshi, M. (1967). Reproduction, larval features and life history of Philine denticulata (J. Adams) (Mollusca—Tectibranchia). Ophelia, 4, 43–84.

    Google Scholar 

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

    Article  Google Scholar 

  • Hughes, H. P. I. (1991). Sand-dwelling opisthobranchs from Hong Kong. Journal of Molluscan Studies, 57, 425–431.

    Article  Google Scholar 

  • Jensen, K. R. (1996). Phylogenetic Systematics and Classification of the Sacoglossa (Mollusca, Gastropoda, Opisthobranchia). Philosophical Transactions: Biological Sciences, 351, 91–122.

    Article  Google Scholar 

  • Jörger, K. M., Neusser, T. P., Haszprunar, G., & Schrödl, M. (2008). Undersized and underestimated: 3D visualization of the Mediterranean interstitial acochlidian gastropod Pontohedyle milaschewitchii (Kowalevsky, 1901). Organisms, Diversity and Evolution, 8(3), 194–214.

    Article  Google Scholar 

  • Jörger, K. M., Heß, M., Neusser, T. P., & Schrödl, M. (2009). Sex in the beach: spermatophores, dermal insemination and 3D sperm ultrastructure of the aphallic mesopsammic Pontohedyle milaschewitchii (Acochlidia, Opisthobranchia, Gastropoda). Marine Biology, 156, 1159–1170.

    Article  Google Scholar 

  • Jörger, K. M., Stöger, I., Kano, Y., Fukuda, H., Knebelsberger, T., & Schrödl, M. (2010a). On the origin of Acochlidia and other enigmatic euthyneuran gastropods, with implications for the systematics of Heterobranchia. BMC Evolutionary Biology, 10, 323. doi:10.1186/1471-2148-10-323.

    Article  Google Scholar 

  • Jörger, K. M., Kristof, A., Klussmann-Kolb, A., & Schrödl, M. (2010b). Redescription of the meiofaunal gastropod Parhedyle cryptophthalma (Acochlidia, Panpulmonata), with focus on nervous system and sensory organs. Spixiana, 33(2), 161–288.

    Google Scholar 

  • Karlsson, A., & Haase, M. (2002). The enigmatic mating behaviour and reproduction of a simultaneous hermaphrodite, the nudibranch Aeolidiella glauca (Gastropoda, Opisthobranchia). Canadian Journal of Zoology, 80, 260–270.

    Article  Google Scholar 

  • Klussmann-Kolb, A. (2001). Comparative investigation of the genital systems in the Opisthobranchia (Mollusca, Gastropoda) with special emphasis on the nidamental glandular system. Zoomorphology, 120, 215–235.

    Article  Google Scholar 

  • Klussmann-Kolb, A., & Klussmann, A. (2003). A new species of Gastropteridae (Gastropoda, Opisthobranchia, Cephalaspidea) from tropical Northeast Australia. Zootaxa, 156, 1–12.

    Google Scholar 

  • Klussmann-Kolb, A., Dinapoli, A., Kuhn, K., Streit, B., & Albrecht, C. (2008). From sea to land and beyond—new insights into the evolution of euthyneuran Gastropoda (Mollusca). BMC Evolutionary Biology, 8(57). doi:10.1186/1471-2148-8-57

  • Kocot, K. M., Cannon, J. T., Todt, T., Citarella, M. R., Kohn, A. B., Meyer, A., Santos, S. R., Schander, C., Moroz, L. L., Lieb, B., & Halanych, K. M. (2011). Phylogenomics reveals deep molluscan relationships. Nature, 447, 452–456. doi:10.1038/nature10382.

  • Kress, A. (1985). The male copulatory apparatus in an opisthobranch mollusc, Runcina. Tissue & Cell, 17(2), 215–226.

    Article  CAS  Google Scholar 

  • Lemche, H. (1956). The anatomy and histology of Cylichna (Gastropoda: Tectibranchia). Spolia Zoologica Musei Hauniensis, 16, 1–278.

    Google Scholar 

  • Maeda, T., Kajita, M., Maruyama, T., & Hirano, Y. (2010). Molecular phylogeny of the Sacoglossa, with a discussion of gain and loss of kleptoplasty in the evolution of the group. The Biological Bulletin, 219, 17–26.

    PubMed  CAS  Google Scholar 

  • Malaquias, M. A. E., Mackenzie-Dodds, J., Bouchet, P., Gosliner, T., & Reid, D. G. (2009). A molecular phylogeny of the Cephalaspidea sensu lato (Gastropoda: Euthyneura): Architectibranchia redefined and Runcinacea reinstated. Zoologica Scripta, 38, 23–41.

    Article  Google Scholar 

  • Marcus, Er. (1953a). Three Brazilian Sand-Opisthobranchia. Boletim da Faculdade de Filosofia, Ciências e Letras. Universidade de São Paulo, 164, 165–203.

    Google Scholar 

  • Marcus, Ev. (1953b). The opisthobranch Pseudovermis from Brazil. Boletim da Faculdade de Filosofia, Ciências e Letras. Universidade de São Paulo, 165, 109–127.

    Google Scholar 

  • Marcus, Er. (1959). Eine neue Gattung der Philinoglossacea. Kieler Meeresforschung, 15, 117–119.

    Google Scholar 

  • Marcus, Er., & Marcus, Ev. (1954). Über Philinoglossacea und Acochlidiacea. Kieler Meeresforschung, 10, 215–223.

    Google Scholar 

  • Marcus, Ev., & Marcus, Er. (1958). Opisthobranchia aus dem Schill von Helgoland. Kieler Meeresforschung, 14, 91–96.

    Google Scholar 

  • Martínez, E., Ballesteros, M., Ávila, C., Dantart, L., & Cimino, G. (1993). La familia Aglajidae (Opisthobranchia: Cephalaspidea) in the Iberian Peninsula. Iberus, 11(1), 15–29.

    Google Scholar 

  • Martynov, A. V., & Schrödl, M. (2011). Phylogeny and evolution of corambid nudibranchs (Mollusca: Gastropoda). Zoological Journal of the Linnean Society, 163, 585–604. doi:10.1111/j.1096-3642.2011.00720.x.

    Google Scholar 

  • Martynov, A. V., Brenzinger, B., Hooker, Y., & Schrödl, M. (2011). 3D-Anatomy of a new tropical Peruvian nudibranch gastropod species, Corambe mancorensis, and novel hypotheses on dorid gill ontogeny and evolution. Journal of Molluscan Studies, 77, 129–141.

    Article  Google Scholar 

  • Mikkelsen, P. M. (1996). The evolutionary relationships of Cephalaspidea s.l. (Gastropoda: Opisthobranchia): a phylogenetic analysis. Malacologia, 37(2), 375–442.

    Google Scholar 

  • Mikkelsen, P. M. (1998). Cylindrobulla and Ascobulla in the western Atlantic (Gastropoda, Opisthobranchia, Sacoglossa): Systematic review, description of a new species, and phylogenetic reanalysis. Zoologica Scripta, 27(1), 49–71.

    Article  Google Scholar 

  • Mikkelsen, P. M. (2002). Shelled opisthobranchs. Advances in Marine Biology, 42, 67–136.

    Article  PubMed  Google Scholar 

  • Morse, M. P. (1976). Hedylopsis riseri n. sp., a new interstitial mollusc from the New England coast (Opisthobranchia, Acochlidiacea). Zoologica Scripta, 5, 221–229.

    Article  Google Scholar 

  • Morse, M. P. (1987). Distributions and ecological adaptations of interstitial molluscs in Fiji. American Malacological Bulletin, 5, 281–286.

    Google Scholar 

  • Neusser, T. P., & Schrödl, M. (2007). Tantulum elegans reloaded: a computer-based 3D-visualization of the anatomy of a Caribbean freshwater acochlidian gastropod. Invertebrate Biology, 126, 18–39.

    Article  Google Scholar 

  • Neusser, T. P., Heß, M., Haszprunar, G., & Schrödl, M. (2006). Computer-based three-dimensional reconstruction of the anatomy of Microhedyle remanei (Marcus, 1953), an interstitial acochlidian gastropod from Bermuda. Journal of Morphology, 267, 231–247.

    Article  PubMed  Google Scholar 

  • Neusser, T. P., Martynov, A. V., & Schrödl, M. (2009a). Heartless and primitive? 3D reconstruction of the polar acochlidian gastropod Asperspina murmanica. Acta Zoologica, 90, 228–245.

    Article  Google Scholar 

  • Neusser, T. P., Heß, M., & Schrödl, M. (2009b). Tiny but complex—interactive 3D visualization of the interstitial acochlidian gastropod Pseudunela cornuta (Challis, 1970). Frontiers in Zoology, 6(20). doi:10.1186/1742-9994-6-20

  • Neusser, T. P., Jörger, K. M., & Schrödl, M. (2011a). Cryptic speciation in tropic sands—interactive 3D anatomy, molecular phylogeny and evolution of meiofaunal Pseudunelidae (Gastropoda, Acochlidia). PLoS ONE, 6(8). doi:10.1186/1742-9994-6-20.

  • Neusser, T. P., Fukuda, H., Jörger, K. M., Kano, Y., & Schrödl, M. (2011b). Sacoglossa or Acochlidia? 3D-reconstruction, molecular phylogeny and evolution of Aitengidae (Gastropoda, Heterobranchia). Journal of Molluscan Studies, 77, 332–350.

    Article  Google Scholar 

  • Padilla, D. K. (1998). Inducible phenotypic plasticity of the radula in Lacuna (Gastropoda: Littorinidae). Veliger, 41, 201–204.

    Google Scholar 

  • Perrier, R., & Fischer, H. (1911). Recherches anatomiques et histologiques sur la cavité palléale et ses dépendances chez les Bulléens. Annales des Sciences Naturelles (Zoologie), 14, 1–190.

    Google Scholar 

  • Reid, D. G., & Mak, Y. M. (1999). Indirect evidence for ecophenotypic plasticity in radular dentition of Littoraria species (Gastropoda: Littorinidae). Journal of Molluscan Studies, 65, 355–370.

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Risbec, J. (1951). Notes sur les Tectibranches de Nouvelle-Calédonie. Journal de la Société des Océanistes, 7, 123–158.

    Article  Google Scholar 

  • Rückert, I.-M., Altnöder, A., & Schrödl, M. (2008). Computer-based 3D anatomical reconstruction and systematic placement of the mesopsammic gastropod Platyhedyle denudata Salvini-Plawen, 1973 (Opisthobranchia, Sacoglossa). Organisms, Diversity and Evolution, 8, 358–367.

    Article  Google Scholar 

  • Rudman, W. B. (1972a). On Melanochlamys Cheeseman, 1881, a Genus of the Aglajidae (Opisthobranchia, Gastropoda). Pacific Science, 26, 50–62.

    Google Scholar 

  • Rudman, W. B. (1972b). The genus Philine (Opisthobranchia, Gastropoda). Proceedings of the Malacological Society of London, 40, 171–187.

    Google Scholar 

  • Rudman, W. B. (1974). A comparison of Chelidonura, Navanax and Aglaja with other genera of the Aglajidae (Opisthobranchia: Gastropoda). Zoological Journal of the Linnean Society, 54, 185–212.

    Article  Google Scholar 

  • Rudman, W. B. (1978). A new species and genus of the Aglajidae and the evolution of the philinacean opisthobranch molluscs. Zoological Journal of the Linnean Society, 62(1), 89–107.

    Article  Google Scholar 

  • Rudman, W. B. (1998). (December 18) Philine trapezia Hedley, 1902. In: Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/factsheet/philtrap.

  • Rudman, W. B. (2001). (June 8) Yellow gland—Aglajidae. In: Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/factsheet/yellink.

  • Rundell, R. J., & Leander, B. S. (2010). Masters of miniaturization: Convergent evolution among interstitial eukaryotes. Bioessays, 32, 430–437.

    Article  PubMed  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 

  • Salvini-Plawen, Lv. (1973). Zur Kenntnis der Philinoglossacea und der Acochlidiacea mit Platyhedylidae fam. nov. (Gastropoda, Cephalaspidea). Zeitschrift für zoologische Systematik und Evolutionsforschung, 11, 110–133.

    Article  Google Scholar 

  • Salvini-Plawen, Lv. (1984). Notes on molluscan meiofauna from Plymouth. Journal of the Marine Biological Association of the United Kingdom, 64, 497–502.

    Article  Google Scholar 

  • Salvini-Plawen, Lv. (1991). The status of the Rhodopidae (Gastropoda: Euthyneura). Malacologia, 32, 301–311.

    Google Scholar 

  • Schrödl, M. (2006). (February 9) Techniques for collecting interstitial opisthobranchs. In: Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/factsheet/inteextr.

  • Schrödl, M., & Neusser, T. P. (2010). Towards a phylogeny and evolution of Acochlidia. Zoological Journal of the Linnean Society, 158, 124–154.

    Article  Google Scholar 

  • Schrödl, M., Jörger, K. M., Klussmann-Kolb, A., & Wilson, N. G. (2011a). Bye bye "Opisthobranchia"! A review on the contribution of mesopsammic sea slugs to euthyneuran systematics. Thalassas, 27(2), 101–112.

    Google Scholar 

  • Schrödl, M., Jörger, K. M., & Wilson, N. G. (2011b). A reply to Medina et al. (2011): Crawling through time: Transition of snails to slugs dating back to the Paleozoic based on mitochondrial phylogenomics. Marine Genomics, 4(4), 301–303.

    Article  Google Scholar 

  • Sleeper, H. L., Paul, V. L., & Fenical, W. (1980). Alarm pheromones from the marine opisthobranch Navanax inermis. Journal of Chemical Ecology, 6(1), 57–70.

    Article  CAS  Google Scholar 

  • Smith, S. A., Wilson, N. G., Goetz, F. E., Feehery, C., Andrade, S. C. S., Rouse, G. W., Giribet, G., & Dunn, C. W. (2011). Resolving the evolutionary relationships of molluscs with phylogenomic tools. Nature, 480, 364–367. doi:10.1038/nature10526.

  • Spurr, A. R. (1969). A low-viscosity resin embedding medium for electron microscopy. Journal of Ultrastructural Research, 26, 31–43.

    Article  CAS  Google Scholar 

  • Staubach, S., Schützner, P., Croll, R. P., & Klussmann-Kolb, A. (2008). Innervation patterns of the cerebral nerves in Haminoea hydatis (Gastropoda: Opisthobranchia): a test for intraspecific variability. Zoomorphology, 127, 203–212.

    Article  Google Scholar 

  • Swedmark, B. (1964). The interstitial fauna of marine sand. Biological Reviews, 39, 1–42.

    Article  Google Scholar 

  • Swedmark, B. (1968). The biology of interstitial Mollusca. Symposium of the Zoological Society of London, 22, 135–149.

    Google Scholar 

  • Swedmark, B. (1971). A review of Gastropoda, Brachiopoda, and Echinodermata in marine meiobenthos. Smithsonian Contributions to Zoology, 76, 41–45.

    Google Scholar 

  • Thiele, J. (1931). Handbuch der Systematischen Weichtierkunde, Teil 2: (Gastropoda: Opisthobranchia: Pulmonata). Vol 2, part 2 (pp. 377–788). Jena: Fischer.

    Google Scholar 

  • Urgorri, V., Cobo, F., & Besteiro, C. (1991). Pseudovermis artabrensis (Nudibranchia: Aeolidoidea), a new species from Galicia, Spain. Journal of Molluscan Studies, 57, 189–197.

    Article  Google Scholar 

  • Valdés, A., Gosliner, T. M., & Ghiselin, M. T. (2010). Chapter 8: Opisthobranchs. In A. Córdoba-Aguilar & J. L. Leonard (Eds.), The Evolution of Primary Sexual Characters in Animals (pp. 148–172). Oxford: Oxford University Press.

    Google Scholar 

  • Vinther, J., Sperling, E. A., Briggs, D. E. G., & Peterson, K. J. (2011). A molecular palaeobiological hypothesis for the origin of aplacophoran molluscs and their derivation from chiton–like ancestors. Proceedings of the Royal Society B: Biological Sciences, 279, 1259–1268. doi:10.1098/rspb.2011.1773.

  • Vonnemann, V., Schrödl, M., Klussmann-Kolb, A., & Wägele, H. (2005). Reconstruction of the phylogeny of the Opisthobranchia (Mollusca: Gastropoda) by means of 18s and 28s rRNA gene sequences. Journal of Molluscan Studies, 71, 113–125.

    Article  Google Scholar 

  • Wägele, H., & Klussmann-Kolb, A. (2005). Opisthobranchia (Mollusca, Gastropoda)—more than just slimy slugs. Shell reduction and its implications on defence and foraging. Frontiers in Zoology, 2(3). doi:10.1186/1742-9994-2-3

  • Wägele, H., & Willan, R. C. (2000). Phylogeny of the Nudibranchia. Zoological Joumal of the Linnean Society, 130, 83–181.

    Article  Google Scholar 

  • Wägele, H., Ballesteros, M., & Avila, C. (2006). Defensive glandular structures in opisthobranch molluscs—from histology to ecology. Oceanography and Marine Biology: An Annual Review, 44, 197–276.

    Google Scholar 

Download references

Acknowledgments

The 3D reconstruction was financed by a PhD grant to B.B. by the Universität Bayern. V.P. is a PhD scholarship holder from National Council for Scientific and Technological Development (CNPq-Brasil) and the German Academic Exchange Service (DAAD). The field trips to Brazil were financed by a grant of the DFG to M.S. (DFG SCHR 667/3,4). The GeoBioCenter LMU supported us with diving equipment. Luiz R. L. Simone and Carlo M. Cunha (MZSP, São Paulo) are thanked for their collaboration. We are grateful to Martin Heß (LMU, Munich) for his help in creating the interactive 3D model. Two anonymous referees provided constructive criticism on the manuscript.

Author information

Authors and Affiliations

  1. Bavarian State Collection of Zoology, Section Mollusca, Münchhausenstr. 21, 81247, Munich, Germany

    Bastian Brenzinger, Vinicius Padula & Michael Schrödl

  2. Department Biology II and GeoBio-Center, Ludwig-Maximilians-Universität München, Großhaderner Str. 2, 82152, Planegg-Martinsried, Germany

    Bastian Brenzinger, Vinicius Padula & Michael Schrödl

Authors
  1. Bastian Brenzinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vinicius Padula
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Schrödl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bastian Brenzinger.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure S1

(PDF 3.93 mb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brenzinger, B., Padula, V. & Schrödl, M. Insemination by a kiss? Interactive 3D-microanatomy, biology and systematics of the mesopsammic cephalaspidean sea slug Pluscula cuica Marcus, 1953 from Brazil (Gastropoda: Euopisthobranchia: Philinoglossidae). Org Divers Evol 13, 33–54 (2013). https://doi.org/10.1007/s13127-012-0093-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-012-0093-3

Keywords

Search

Navigation