Integrating 3D microanatomy and molecules: Natural history of the pacific freshwater slug strubellia Odhner, 1937 (Heterobranchia: Acochlidia), with description of a new species

Journal of Molluscan Studies

Volumn 77, Issue 4, 2011, Pages 351-374

  Brenzinger, Bastian ^a   Neusser, Timea P ^a   Jörger, Katharina M ^a   Schrödl, Michael ^a  

^a ZOOLOGISCHE STAATSSAMMLUNG MÜNCHEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANATOMY; BIOLOGICAL CHARACTERISTICS; CLADISTICS; COPULATION; FRESHWATER ENVIRONMENT; GENETIC ANALYSIS; MOLECULAR ANALYSIS; MORPHOLOGY; NEW SPECIES; PHYLOGENY; SLUG; TAXONOMY; THREE-DIMENSIONAL MODELING;

SOLOMON ISLANDS [(ISG) MELANESIA]; VANUATU;

ACOCHLIDIIDAE; GASTROPODA; HETEROBRANCHIA; NERITIDAE; PYRAMIDELLOIDEA; SACOGLOSSA; STRUBELLIA;

EID: 80755123459     PISSN: 02601230     EISSN: 14643766     Source Type: Journal    
DOI: 10.1093/mollus/eyr027     Document Type: Conference Paper

References (96)

1. ALTSCHUL, S.F., GISH, W., MILLER, W., MYERS, E.W. &LIPMAN, D.J. 1990. Basic local alignment search tool. Journal ofMolecular Biology, 215: 403-410.
2. ANDREWS, E.A. 1935. The egg capsules of certain Neritidae. Journalof Morphology, 57: 31-59.
3. ARNAUD, P.M., POIZAT, C.L. & SALVINI-PLAWEN, L. VON.1986. Marine-interstitial Gastropoda (including one freshwaterinterstitial species). A faunistic, distributional, and ecologicalsynthesis of the world fauna inhabiting subterranean waters(including the marine interstitial). In: Stygofauna mundi(L. Botoseanu, ed.), pp. 153-165.
4. E.J. Brill/Dr. W. Backhuys,Leiden.BÄUMLER, N., HASZPRUNAR, G. & RUTHENSTEINER, B.2008. 3D interactive microanatomy of Omalogyra atomus (Philippi,1841) (Gastropoda, Heterobranchia, Omalogyridae). Zoosymposia,1: 101-118.
5. BARBER, P.H., PALUMBI, S.R., ERDMANN, M.V. & MOOSA,M.K. 2000. A marine Wallace's line? Nature, 406: 692-693.
6. BARNES, R.S.K. 1994. The brackish-water fauna of northwestern Europe.Cambridge University Press.
7. BAYER, F.M. & FEHLMANN, H.A. 1960. The discovery of afreshwater opisthobranchiate mollusk, Acochlidium amboinenseStrubell, in the Palau Islands. Proceedings of the Biological Society ofWashington, 73: 183-194.
8. BERGH, R. 1895. Die Hedyliden, eine Familie der kladohepatischenNudibranchien. Verhandlungen der k.k. zoologisch-botanischen Gesellschaftin Wien, 45: 1-12.
9. BOER, H.H., SLOT, J.W. & VAN ANDEL, J. 1968. Electronmicroscopical and histochemical observations on the relationbetween medio-dorsal bodies and neurosecretory cells in thebasommatophoran snails Lymnaea stagnalis, Ancylus fluviatilis,Australorbis glabratus and Planorbarius corneus. Zeitschrift fürZellforschung, 87: 435-450.
10. BRENZINGER, B., NEUSSER, T.P., GLAUBRECHT, M.,HASZPRUNAR, G. & SCHRÖDL, M. 2011. Redescription and3-dimensional reconstruction of the limnic acochlidian gastropodStrubellia paradoxa (Strubell, 1892) (Gastropoda, Euthyneura) fromAmbon, Indonesia. Journal of Natural History, 45: 183-209.
11. BÜCKING, G. 1933. Hedyle amboinensis (Strubell). ZoologischeJahrbücher der Abteilung für Systematik, 64: 549-582.
12. CATTANEO-VIETTI, R., ANGELINI, S., GAGGERO, L. &LUCCHETTI, G. 1995. Mineral composition of nudibranchspicules. Journal of Molluscan Studies, 61: 331-337.
13. CHALLIS, D.A. 1968. A new genus and species of the orderAcochlidiacea (Mollusca: Opisthobranchia) from Melanesia.Transactions of the Royal Society of New Zealand Biological Sciences, 10:191-197.
14. CLEMENT, M., POSADA, D. & CRANDALL, K.A. 2000. TCS: acomputer program to estimate gene genealogies. Molecular Ecology,9: 1657-1659.
15. COELHO, R., MALAQUIAS, M.A.E. & CALADO, G. 2006.Calliopaea bellula feeding upon egg-masses of Haminoea orbignyana:oophagy among opisthobranch molluscs. Journal of the MarineBiological Association of the United Kingdom, 86: 423-424.
16. DAYRAT, B. & TILLIER, S. 2002. Evolutionary relationships ofeuthyneuran gastropods (Mollusca): a cladistic re-evaluation ofmorphological characters. Zoological Journal of the Linnean Society,135: 403-470.
17. EDER, B., SCHRÖDL, M. & JÖRGER, K.M. 2011. Systematics andredescription of the European meiofaunal slug Microhedyleglandulifera (Kowalevsky, 1901) (Heterobranchia: Acochlidia):evidence from molecules and morphology. Journal of MolluscanStudies, 77: 388-400.
18. EDGAR, R.C. 2004. MUSCLE: multiple sequence alignment withhigh accuracy and high throughput. Nucleic Acids Research, 32:1792-1797. (Pubitemid 38832724)
19. EDLINGER, K. 1980. Beiträge zur Anatomie, Histologie,Ultrastruktur und Physiologie der chemischen Sinnesorgane einigerCephalaspidea (Mollusca, Opisthobranchia). Zoologischer Anzeiger,205: 90-112.
20. EVANS, T.J. 1951. The alimentary and vascular systems of Alderiamodesta (Lovén) in relation to its ecology. Proceedings of theMalacological Society, 29: 249-258.
21. FAHRNER, A. & HASZPRUNAR, G. 2001. Anatomy andultrastructure of the excretory system of a heart-bearing and aheart-less sacoglossan gastropod (Opisthobanchia, Sacoglossa).Zoomorphology, 121: 85-93.
22. FAHRNER, A. & HASZPRUNAR, G. 2002. Microanatomy,ultrastructure, and systematic significance of the excretory systemand mantle cavity of an acochlidian gastropod (Opisthobranchia).Journal of Molluscan Studies, 68: 87-94.
23. FOLMER, O., BLACK, M., HOEH, W., LUTZ, R. &VRIJENHOEK, R. 1994. DNA primers for amplification ofmitochondrial cytochrome c oxidase subunit I from diversemetazoan invertebrates. Molecular Marine Biology and Biotechnology, 3:294-299.
24. GASCOIGNE, T. 1974. A note on some sacoglossan penial styles(Gastropoda: Opisthobranchia). Zoological Journal of the LinneanSociety, 55: 53-59.
25. GHISELIN, M.T. 1966. Reproductive function and the phylogeny ofopisthobranch gastropods. Malacologia, 3: 327-378.
26. GÖBBELER, K. & KLUSSMANN-KOLB, A. 2007. A comparativeultrastructural investigation of the cephalic sensory organs inOpisthobranchia (Mollusca, Gastropoda). Tissue and Cell, 39:399-414. (Pubitemid 350131477)
27. GOLDING, R.E. 2010. Anatomy in Toledonia warenella n. sp.(Gastropoda: Opisthobranchia: Diaphanidae) visualized bythree-dimensional reconstruction. Invertebrate Biology, 129: 151-164.
28. GOLDING, R.E., PONDER, W.F. & BYRNE, M. 2007. Taxonomyand anatomy of Amphiboloidea (Gastropoda: Heterobranchia:Archaeopulmonata). Zootaxa, 1476: 1-50. (Pubitemid 46833649)
29. GOSLINER, T.M. 1994. Gastropoda: Opisthobranchia. In: Microscopicanatomy of invertebrates. Vol. 5: Mollusca (F.W. HARRISON &A.W. KOHN, eds), pp. 253-355.
30. Wiley-Liss, New York.GOSLINER, T.M. & GHISELIN, M.T. 1984. Parallel evolution inopisthobranch gastropods and its implications for phylogeneticmethodology. Systematic Zoology, 33: 255-274.
31. HAASE, M. & WAWRA, E. 1996. The genital system of Acochlidiumfijiense (Opisthobranchia: Acochlidioidea) and its inferred function.Malacologia, 38: 143-151. (Pubitemid 126171921)
32. HADL, G., KOTHBAUER, H., PETER, R. & WAWRA, E. 1969. Substratwahlversuche mit Microhedyle milaschewitchii Kowalevsky(Gastropoda, Opisthobranchia: Acochlidiacea). Oecologia, 4: 74-82.
33. HASZPRUNAR, G. 1985a. The Heterobranchia-a new concept ofthe phylogeny of the higher Gastropoda. Zeitschrift für zoologischeSystematik und Evolutionsforschung, 23: 15-37.
34. HASZPRUNAR, G. 1985b. The fine morphology of the osphradialsense organs of the Mollusca II. Allogastropoda (Architectonicidae,Pyramidellidae). Philosophical Transactions of the Royal Society ofLondon, Series B, 307: 497-505.
35. HASZPRUNAR, G. 1988. On the origin and evolution of majorgastropod groups, with special reference to the Streptoneura.Journal of Molluscan Studies, 54: 367-441.
36. HASZPRUNAR, G. & HUBER, G. 1990. On the central nervoussystem of Smeagolidae and Rhodopidae, two families questionablyallied with the Gymnomorpha (Gastropoda: Euthyneura). Journalof the Zoological Society of London, 220: 185-199.
37. HAYNES, A. 1988. Notes on the stream neritids (Gastropoda;Prosobranchia) of Oceania. Micronesica, 21: 93-102.
38. HAYNES, A. 2000. The distribution of freshwater gastropods on fourVanuatu islands: Espiritu Santo, Pentecost, Éfate and Tanna(South Pacific). Annals of Limnology, 36: 101-111. (Pubitemid 30457886)
39. HAYNES, A. & KENCHINGTON, W. 1991. Acochlidium fijiensis sp.nov. (Gastropoda: Opisthobranchia: Acochlidiacea) from Fiji.Veliger, 34: 166-171.
40. HOLZNAGEL, W.E. 1998. A nondestructive method for cleaninggastropod radulae from frozen, alcohol-fixed, or dried material.American Malacological Bulletin, 14: 181-183. (Pubitemid 128184967)
41. HUBER, G. 1993. On the cerebral nervous system of marineHeterobranchia (Gastropoda). Journal of Molluscan Studies, 59:381-420. (Pubitemid 2009667)
42. JENSEN, K.R. 1980. A review of sacoglossan diets, with comparativenotes on radular and buccal anatomy. Malacological Review, 13:55-77.
43. JENSEN, K.R. 1981. Observations on feeding methods in someFlorida ascoglossans. Journal of Molluscan Studies, 47: 190-199.
44. JENSEN K.R. 1996. Phylogenetic systematics and classification of theSacoglossa (Mollusca, Gastropoda, Opisthobranchia). PhilosophicalTransactions of the Royal Society of London Series B 351 91-122.
45. JÖRGER, K.M., KRISTOF, A., KLUSSMANN-KOLB, A. &SCHRÖDL, M. 2010b. Redescription of the meiofaunal gastropodParhedyle cryptophthalma (Acochlidia, Panpulmonata), with focus onnervous system and sensory organs. Spixiana, 33: 161-170.
46. JÖRGER, K.M., NEUSSER, T.P., HASZPRUNAR, G. &SCHRÖDL, M. 2008. Undersized and underestimated: 3Dvisualization of the Mediterranean interstitial acochlidiangastropod Pontohedyle milaschewitchii (Kowalevsky, 1901). Organisms,Diversity and Evolution, 8: 194-214.
47. JÖRGER, K.M., STÖGER, I., KANO, Y., FUKUDA, H.,KNEBELSBERGER, T. & SCHRÖDL, M. 2010a. On the originof Acochlidia and other enigmatic euthyneuran gastropods, withimplications for the systematics of Heterobranchia. BMCEvolutionary Biology, 10: doi:10.1186/1471-2148-10-323.
48. KANO, Y. 2009. Hitchhiking behaviour in the obligatory upstreammigration of amphidromous snails. Biology Letters, 5: 465-468.
49. KANO, Y. & FUKUMORI, H. 2010. Predation on hardest molluscaneggs by confamilial snails (Neritidae) and its potential significance inegg-laying site selection. Journal of Molluscan Studies, 76: 360-366.
50. KOHNERT, P., NEUSSER, T.P., JÖRGER, K.M. & SCHRÖDL,M. (2011). Time for sex change! 3D-reconstruction of thecopulatory system of the "aphallic" Hedylopsis ballantinei(Gastropoda, Acochlidia). Thalassas, 27: 113-119.
51. KLUSSMANN-KOLB, A., DINAPOLI, A., KUHN, K., STREIT, B.& ALBRECHT, C. 2008. From sea to land and beyond-newinsights into the evolution of euthyneuran Gastropoda (Mollusca).BMC Evolutionary Biology, 8: doi: 10.1186/1471-2148
52. 8-57.KÜTHE, P. 1935. Organisation und systematische Stellung desAcochlidium paradoxum Strubell. Zoologische Jahrbücher der Abteilung fürSystematik, 66: 513-540.
53. MCDOWALL, R.M. 2007. On amphidromy, a distinct form ofdiadromy in aquatic organisms. Fish and Fisheries, 8: 1-13.
54. MARCUS, E.D.B.-R. 1976. A taxonomic survey of the genus ToledoniaDall, 1902 (Opisthobranchia, Diaphanidae). Zoologica Scripta, 5:25-33.
55. MEIER, R., SHIYANG, K., VAIDYA, G. & NG, P.K.L. 2006. DNAbarcoding and taxonomy in diptera: A tale of high intraspecificvariability and low identification success. Systematic Biology, 55:715-728.
56. MIKKELSEN, P.M. 1998. Cylindrobulla and Ascobulla in the westernAtlantic (Gastropoda, Opisthobranchia, Sacoglossa): Systematicreview, description of a new species, and phylogenetic reanalysis.Zoologica Scripta, 27: 49-71. (Pubitemid 28232346)
57. MYERS, M.J., MEYER, C.P. & RESH, V.H. 2000. Neritid andthiarid gastropods from French Polynesian streams: howreproduction (sexual, parthenogenetic) and dispersal (active,passive) affect population structure. Freshwater Biology, 44: 535-545. (Pubitemid 30442033)
58. NEUSSER T.P., FUKUDA H., JÖRGER K.M., KANO Y. &SCHRÖDL, M. 2011a. Sacoglossa or Acochlidia? 3Dreconstruction, molecular phylogeny and evolution of Aitengidae(Heterobranchia: Gastropoda Journal of Molluscan Studies 77 332-350.
59. NEUSSER, T.P., HEb, M. & SCHRÖDL, M. 2009a. Tiny butcomplex-interactive 3D visualization of the interstitial acochlidiangastropod Pseudunela cornuta (Challis, 1970). Frontiers in Zoology, 6.doi: 10.1186/1742-9994-
60. 6-20.NEUSSER, T.P., JÖRGER, K.M. & SCHRÖDL, M. 2007.Exploring cerebral features in Acochlidia (Gastropoda:Opisthobranchia). Bonner Zoologische Beiträge, 55: 301-310.
61. NEUSSER, T.P., JÖRGER, K.M. & SCHRÖDL, M. 2011b. Crypticspecies in tropic sands-interactive 3D anatomy, molecularphylogeny and evolution of meiofaunal Pseudunelidae(Gastropoda, Acochlidia). PLoS ONE, 6(8): e23313. doi: 10.1371/journal.pone.0023313.
62. NEUSSER, T.P., MARTYNOV, A.V. & SCHRÖDL, M. 2009b.Heartless and primitive? 3D reconstruction of the polar acochlidiangastropod Asperspina murmanica. Acta Zoologica, 90: 228-245.
63. NEUSSER, T.P. & SCHRÖDL, M. 2007. Tantulum elegans reloaded: acomputer-based 3D-visualization of the anatomy of a Caribbeanfreshwater acochlidian gastropod. Invertebrate Biology, 126: 18-39. (Pubitemid 46535435)
64. NEUSSER, T.P. & SCHRÖDL, M. 2009. Between Vanuatu tides: 3Danatomical reconstruction of a new brackish water acochlidiangastropod from Espiritu Santo. Zoosystema, 31: 453-469.
65. ODHNER, N.HJ. 1937. Strubellia, eine neue Gattung derAcochlidiacea. Zoologischer Anzeiger, 120: 237-238.
66. PONDER, W.F. 1986. Glacidorbidae (Glacidorbacea:Basommatophora), a new family and superfamily of operculatefreshwater gastropods. Zoological Journal of the Linnean Society, 87:53-83.
67. PONDER, W.F. & AVERN, G.J. 2000. The Glacidorbidae (Mollusca:Gastropoda: Heterobranchia) of Australia. Records of the AustralianMuseum, 52: 307-353.
68. POSADA, D. 2008. jModelTest: Phylogenetic model averaging.Molecular Biology and Evolution, 25: 1253-1256. (Pubitemid 351882013)
69. RANKIN, J.J. 1979. A freshwater shell-less mollusc from theCaribbean: structures, biotics and contribution to a newunderstanding of the Acochlidioidea. Royal Ontario Museum LifeSciences Contributions, 116: 1-123.
70. RICHARDSON, K.C., JARETT, L. & FINKE, E.H. 1960.Embedding in epoxy resins for ultrathin sectioning in electronmicroscopy. Stain Technology, 35: 313-323.
71. RIEGER, R.M. & STERRER, W. 1975. New spicular skeletons inTurbellaria, and the occurrence of spicules in marine meiofauna.Zeitschrift für zoologische Systematik und Evolutionsforschung, 13:249-278.
72. RUTHENSTEINER, B. 2008. Soft Part 3D visualization by serialsectioning and computer reconstruction. Zoosymposia, 1: 63-100.
73. RUTHENSTEINER, B. & HEb, M. 2008. Embedding 3D models ofbiological specimens in PDF publications. Microscopy Research andTechnique, 71: 778-786.
74. SALEUDDIN, A.S.M., ASHTON, M.L. & KHAN, H.R. 1997. Anelectron microscopic study of the endocrine dorsal bodies inreproductively active and inactive Siphonaria pectinata (Pulmonata:Mollusca). Tissue and Cell, 29: 267-275. (Pubitemid 27268107)
75. SCHMEKEL, L. & PORTMANN, A. 1982. Opisthobranchia desMittelmeeres. Nudibranchia und Saccoglossa. Heidelberg,Springer-Verlag, Berlin.
76. SCHRÖDL, M., JÖRGER, K.M., KLUSSMANN-KOLB, A. &WILSON, N.G. 2011. Bye bye "Opisthobranchia"! A review onthe contribution of mesopsammic sea slugs to euthyneuransystematics. Thalassas., 27: 101-112.
77. SCHRÖDL, M. & NEUSSER, T.P. 2010. Towards a phylogeny andevolution of Acochlidia. Zoological Journal of the Linnean Society, 158:124-154.
78. SCHRÖDL, M. & WÄGELE, H. 2001. Anatomy and histology ofCorambe lucea Marcus, 1959 (Gastropoda, Nudibranchia,Doridoidea), with a discussion of the systematic position ofCorambidae. Organisms, Diversity and Evolution, 1: 3-16. (Pubitemid 33706573)
79. SCHRÖDL, M., WÄGELE, H. & WILLAN, R.C. 2001. Taxonomicredescription of the Doridoxidae (Gastropoda: Opisthobranchia),an enigmatic family of deep water nudibranchs, with discussion ofbasal nudibranch phylogeny. Zoologischer Anzeiger, 240: 83-97. (Pubitemid 32511868)
80. SIMON, C., FRATI, F., BECKENBACH, A., CRESPI, B., LIU, H.& FLOOK, P. 1994. Evolution, weighting, and phylogenetic utilityof mitochondrial gene sequences and a compilation of conservedpolymerase chain reaction primers. Annals of the Entomological Societyof America, 87: 651-701.
81. SOMMERFELDT, N. & SCHRÖDL, M. 2005. Microanatomy ofHedylopsis ballantinei, a new interstitial acochlidian gastropod fromthe Red Sea, and its significance for phylogeny. Journal of MolluscanStudies, 71: 153-165. (Pubitemid 40689734)
82. SPURR, A.R. 1969. A low-viscosity resin embedding medium forelectron microscopy. Journal of Ultrastructural Research, 26: 31-43.
83. STAMATAKIS, A. 2006. RAxML-VI-HPC: maximumlikelihood-based phylogenetic analyses with thousands of taxa andmixed models. Bioinformatics, 22: 2688-2690. (Pubitemid 44642609)
84. STARMÜHLNER, F. 1976. Beiträge zur Kenntnis derSübwasser-Gastropoden pazifischer Inseln. Annalen desNaturhistorischen Museums Wien, 80: 473-656.
85. STOTHARD, J.R. & ROLLINSON, D. 1997. Partial DNAsequences from the mitochondrial cytochrome oxidase subunit I(COI) gene can differentiate the intermediate snail hosts Bulinusglobosus and B. nasutus (Gastropoda: Planorbidae). Journal of NaturalHistory, 31: 727-737. (Pubitemid 27320087)
86. STRUBELL, A. 1892. Sitzung der naturwissenschaftlichen Sektionvom 13. Juni 1892. Verhandlungen des naturhistorischen Vereins derpreussischen Rheinlande, 49: 56-62.
87. SWEDMARK, B. 1968. The biology of interstitial mollusca. Symposiumof the Zoological Society of London, 22: 135-149.
88. SWENNEN, C. & BUATIP, S. 2009. Aiteng ater, new genus, newspecies, an amphibious and insectivorous sea slug that is difficult toclassify [Mollusca: Gastropoda: Opisthobranchia: Sacoglossa(?):Aitengidae, new family]. Raffles Bulletin of Zoology, 57: 495-500.
89. THOMPSON, T.E. 1976. Biology of opisthobranch molluscs. Vol. 1. RaySociety, London.
90. WÄGELE, H. & KLUSSMANN-KOLB, A. 2005. Opisthobranchia(Mollusca, Gastropoda)-more than just slimy slugs. Shellreduction and its implications on defence and foraging. Frontiers inZoology, 2: 3. doi: 10.1186/1742-9994-
91. 2-3.WAWRA, E. 1974. The rediscovery of Strubellia paradoxa (Strubell)(Gastropoda: Euthyneura: Acochlidiacea) on the Solomon Islands.Veliger, 17: 8-10.
92. WAWRA, E. 1979. Acochlidium sutteri nov. spec. (Gastropoda, Opisthobranchia, Acochlidiacea) von Sumba, Indonesien. Annalendes Naturhistorischen Museums Wien, 82: 595-604.
93. WAWRA, E. 1980. Acochlidium bayerfehlmanni spec. nov. (Gastropoda:Opisthobranchia: Acochlidiacea) from Palau Islands. Veliger, 22:215-220.
94. WAWRA, E. 1987. Zur Anatomie einiger Acochlidia (Gastropoda, Opisthobranchia) mit einer vorläufigen Revision des Systems undeinem Anhang über Platyhedylidae (Opisthobranchia, Ascoglossa).Dissertation No. 17335. Universität Wien, Vienna.
95. WAWRA, E. 1988. Strubellia paradoxa (Strubell 1892) (Gastropoda: Opisthobranchia) von den Salomon-Inseln. Zoologischer Anzeiger,220: 163-172.
96. WAWRA, E. 1989. Zur Kenntnis der interstitiellen OpisthobranchierartHedylopsis spiculifera (Kowalevsky) (Mollusca, Gastropoda). ZoologicaScripta, 18: 397-403.