3D-microanatomy of the mesopsammic Pseudovermis salamandrops Marcus, 1953 from Brazil (Nudibranchia, Gastropoda)
Tóm tắt
Species of the nudibranch Pseudovermidae Thiele, 1931 are rare but conspicuous inhabitants of the marine mesopsammon. Their characteristic vermiform body with reduced cerata and acorn-shaped head lacking appendages is well adapted to life in the interstices of sand grains. Traditionally, species descriptions are based mainly on external morphology and radula characteristics; knowledge on their anatomy is scarce. Here we provide the first microanatomical redescription of a member of Pseudovermidae based on 3D-reconstruction from histological semi-thin section series. The present study on Pseudovermis salamandrops Marcus, 1953 reveals several discrepancies to the original description especially within the complex triaulic genital system (i.e., absence of a connection between vas deferens and kidney, presence of a receptaculum seminis and a large muscular penial sheath gland). We also add microanatomical details such as the presence of gastroesophageal ganglia in the central nervous system, described for the first time in Pseudovermidae. Concluding from the nematocysts found in the cnidosacs of P. salamandrops, this species is a cnidarivore which likely preys on various meiofaunal cnidarians. We show that microanatomical redescriptions of poorly known Pseudovermidae are needed to gather comparative data as a backbone to place these neglected meiofaunal slugs in a phylogeny and trace their evolutionary pathway into the mesopsammon. Traditional characters used for species delineation are insufficient to diagnose Pseudovermis and an integrative approach is needed to reliably address pseudovermid diversity in the future.
Tài liệu tham khảo
Alejandrino A (2007) Phylogeny of Aeolidacea (Gastropoda: Nudibranchia). Abstract, World Congress of Malacology, Antwerp, Belgium. http://www.unitasmalacologica.org/congress/WCM2007abstracts.pdf
Arnaud PM, Poizat C, Salvini-Plawen L (1986) Marine-interstitial Gastropoda (including one freshwater interstitial species). In: Botosaneanu L (ed) Stygofauna Mundi, vol. 1. Brill/Backhuys, Leiden, pp 153–161
Boaden PJ (1961) Littoral interstital species form Anglesey representing 3 families new to Britain. Nature 191:512
Bouchet P, Rocroi JP (2005) Classification and nomenclator of gastropod families. Malacologia 47:1–368
Bouillon J, Grohmann PA (1994) A new interstitial stolonal hydroid Nannocoryne gen. nov. mammylia sp. nov. (Hydroidomedusae, Anthomedusae, Corynidae). Cah Biol Mar 35:431–439
Brenzinger B, Wilson NG, Schrödl M (2011) 3D microanatomy of a gastropod ‘worm’, Rhodope rousei sp. nov. from Southern Australia. J Molluscan Stud 77:375–387
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. Front Zool 10:37
Brenzinger B, Padula V, Schrödl M (2013b) 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
Carmona L, Pola M, Gosliner TM, Cervera JL (2013) A tale that morphology fails to tell: A molecular phylogeny of Aeolidiidae (Aeolidida, Nudibranchia, Gastropoda). PLoS ONE 8:e63000
Carroll DJ, Kempf SC (1994) Changes occur in the central nervous system of the nudibranch Berghia verrucicornis (Mollusca, Opisthobranchia) during metamorphosis. Biol Bull 186:202–212
Challis DA (1969) New species of Pseudovermis (Opisthobranchia: Aeolidacea) from New Zealand and the Solomon Islands. Trans Roy Soc NZ 11:153–165
DaCosta S, Cunha CM, Simone LRL, Schrödl M (2007) Computer-based 3-dimensional reconstruction of major organ systems of a new aeolid nudibranch subspecies, Flabellina engeli lucianae, from Brazil (Gastropoda: Opisthobranchia). J Molluscan Stud 73:339–353
Eder B, Schrödl M, Jörger KM (2011) Systematics and redescription of the european meiofaunal slug Microhedyle glandulifera (Kowalevsky, 1901) (Heterobranchia: Acochlidia): evidence from molecules and morphology. J Molluscan Stud 77:388–400
Fize A (1961) Note préliminaire sur Pseudovermis setensis n. sp., mollusque opisthobranche eolidien mesopsammique de la côte languedocienne. Bull Soc Zool France 86:253–260
Ghiselin MT (1965) Reproductive function and the phylogeny of opisthobranch gastropods. Malacologia 3:327–378
Graham A (1938) The structure and function of the alimentary canal of aeolid molluscs, with a discussion on their nematocysts. Trans Roy Soc Edinb 59:267–307
Grosvenor GH (1903) On the nematocysts of Aeolids. Proc R Soc Lond 72:462–486
Hamatani I, Nunomura N (1973) A new species of the interstital eolidacean genus Pseudovermis (Opisthobranchia) from Kii, Middle Japan. Publ Seto Mar Biol Lab 21:67–71
Haszprunar G (1985) The Heterobranchia—a new concept of the phylogeny of the higher Gastropoda. Z Zool Syst Evolutionsforsch 23:15–37
Huber G (1993) On the cerebral nervous system of marine Heterobranchia (Gastropoda). J Molluscan Stud 59:381–420
Hughes HPI (1991) Sand-dwelling opisthobranchs from Hong-Kong. J Molluscan Stud 57:425–431
Jörger KM, Schrödl M (2013) How to describe a cryptic species? Practical challenges of molecular taxonomy. Front Zool 10:59
Jörger KM, Neusser TP, Haszprunar G, Schrödl M (2008) Undersized and underestimated: 3D-visualization of the Mediterranean interstitial acochlidian gastropod Pontohedyle milaschewitchii (Kowalevsky, 1901). Org Divers Evol 8:194–214
Jörger KM, Heß M, Neusser TP, Schrödl M (2009) Sex in the beach: spermatophores, dermal insemination and 3D sperm ultrastructure of the aphallic mesopsammic Pontohedyle milaschewitchii (Acochlidia, Opisthobranchia, Gastropoda). Mar Biol 156:1159–1170
Jörger KM, 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 Evol Biol 10:323
Jörger KM, Norenburg JL, Wilson NG, Schrödl M (2012) Barcoding against a paradox? Combined molecular species delineations reveal multiple cryptic lineages in elusive meiofaunal sea slugs. BMC Evol Biol 12:245
Kälker H, Schmekel L (1976) Structure and function of cnidosac of Aeolidoidea (Gastropoda, Nudibranchia). Zoomorphologie 86:41–60
Klussmann-Kolb A, Croll R, Staubach S (2013) Use of axonal projection patterns for the homologisation of cerebral nerves in Opisthobranchia, (Mollusca, Gastropoda). Front Zool 10:20
Kowalevsky A (1901) Études anatomiques sur le genre Pseudovermis. Mem Acad Imp Sci St Petersbourg 12:1–28
Kristof A, Klussmann-Kolb A (2010) Neuromuscular development of Aeolidiella stephanieae Valdez, 2005 (Mollusca, Gastropoda, Nudibranchia). Front Zool 7:24
Marcus E (1953) The opisthobranch Pseudovermis from Brazil. Univ Sao Paulo Fac Filos Cienc E Letras Bol Zool 18:109–127
Marcus E, Marcus E (1955) Über Sand-Opisthobranchia. Kiel Meeresforsch 11:230–243
Martin R (2003) Management of nematocysts in the alimentary tract and in cnidosacs of the aeolid nudibranch gastropod Cratena peregrina. Mar Biol 143:533–541
Martin R, Hess M, Schrödl M, Tomaschko K-H (2009) Cnidosac morphology in dendronotacean and aeolidacean nudibranch molluscs: from expulsion of nematocysts to use in defense? Mar Biol 156:261–268
Martin R, Tomaschko K-H, Heß M, Schrödl M (2010) Cnidosac-related structures in Embletonia (Mollusca, Nudibranchia) compared with dendronotacean and aeolidacean species. Open Mar Biol J 4:96–100
Martynov A, Schrödl M (2011) Phylogeny and evolution of corambid nudibranchs (Mollusca: Gastropoda). Zool J Linnean Soc 163:585–604
Neusser TP, Schrödl M (2007) Tantulum elegans reloaded: a computer-based 3D-visualization of the anatomy of a Caribbean freshwater acochlidian gastropod. Invertebr Biol 126:18–39
Neusser TP, 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. J Morphol 267:231–247
Neusser TP, Heß M, Schrödl M (2009a) Tiny but complex–interactive 3D visualization of the interstitial acochlidian gastropod Pseudunela cornuta (Challis, 1970). Front Zool 6:20
Neusser TP, Martynov AV, Schrödl M (2009b) Heartless and primitive? 3D reconstruction of the polar acochlidian gastropod Asperspina murmanica. Acta Zool (Stock) 90:228–245
Neusser TP, Jörger KM, Schrödl M (2011) Cryptic species in tropic sands–interactive 3D anatomy, molecular phylogeny and evolution of meiofaunal Pseudunelidae (Gastropoda, Acochlidia). PLoS ONE 6:e23313
Poizat C (1983) Mesopsammic opisthobranchs from the Provencal Coast (Marseilles, Bouches du Rhone, France): long term variations of the populations. J Molluscan Stud 12A:126–135
Pola M, Gosliner TM (2010) The first molecular phylogeny of cladobranchian opisthobranchs (Mollusca, Gastropoda, Nudibranchia). Mol Phylogenet Evol 56:931–941
Richardson KC, Jarett L, Finke EH (1960) Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35:313–323
Rivest BR (1984) Copulation by hypodermic injection in the nudibranchs Palio zesterae and P. dubia (Gastropoda, Opisthobranchia). Biol Bull 167:543–554
Rückert I, Altnöder A, Schrödl M (2008) Computer-based 3D anatomical reconstruction and systematic placement of the mesopsammic gastropod Platyhedyle denudata Salvini-Plawen, 1973 (Opisthobranchia, Sacoglossa). Org Divers Evol 8:358–367
Rundell RJ, Leander BS (2010) Masters of miniaturization: convergent evolution among interstitial eukaryotes. Bioessays 32:430–437
Ruthensteiner B (2008) Soft part 3D visualization by serial sectioning and computer reconstruction. Zoosymposia 1:63–100
Salvini-Plawen L (1991) Pseudovermis thompsoni new species (Nudibranchia, Aeolidoidea) from the Northern Adriatic Sea. J Molluscan Stud 57:179–187
Salvini-Plawen L, Rao GC (1973) 3 new mesopsammic representatives from Bay of Bengal–species of Anthohydra gen. nov. (Hydrozoa) and of Pseudovermis (Gastropoda). Z Morph Tiere 74:231–240
Salvini-Plawen L, Sterrer W (1968) Zur Kenntnis der mesopsammalen Gattung Pseudovermis (Gastropoda, Nudibranchia). Helg Meeresun 18:69–77
Schmekel L (1985) Aspects of evolution within the opisthobranchs. In: Trueman ER, Clarke MS (eds) The Mollusca, vol. 10: evolution. Acad Press, London, pp 221–267
Schmekel L, Portmann A (1982) Opisthobranchia des Mittelmeeres. Nudibranchia und Saccoglossa. Fauna e Flora del Golfo di Napoli, 40. Springer, Berlin, 410 pp
Schrödl M (2006) Techniques for collecting interstitial opisthobranchs. Available at http://www.seaslugforum.net/factsheet/inteextr Sydney
Schrödl M, Jörger KM, Klussmann-Kolb A, Wilson NG (2011) Bye bye ‘Opisthobranchia’! A review on the contribution of mesopsammic sea slugs to euthyneuran systematics. Thalassas 27:101–112
Swedmark B (1964) The interstitial fauna of marine sand. Biol Rev 39:1–42
Swedmark B (1968) The biology of interstitial Mollusca. Symp Zool Soc Lond 22:135–149
Tardy J (1970) Contribution à l’étude des métamorphoses chez les nudibranches. Ann Sci Nat Zool Biol Animale 12:299–370
Tardy J (1974) Morphogenese du systéme nerveux chez les mollusques nudibranches. Haliotis 4:61–75
Thiele J (1931) Handbuch der systematischen Weichtierkunde. Vol. 2. Fischer Verlag, Jena
Urgorri V, Cobo F, Besteiro C (1991) Pseudovermis artabrensis (Nudibranchia, Aeolidoidea), a new species from Galicia, Spain. J Molluscan Stud 57:189–197
Wägele H, Klussmann-Kolb A (2005) Opisthobranchia (Mollusca, Gastropoda)–more than just slimy slugs. Shell reduction and its implications on defence and foraging. Front Zool 2:1–18
Wägele H, Willan RC (2000) Phylogeny of the Nudibranchia. Zool J Lin Soc 130:83–181
Wägele H, Klussmann-Kolb A, Verbeek E, Schrödl M (2014) Flashback and foreshadowing—a review of the taxon Opisthobranchia. Org Divers Evol 14:133–149
Westheide W (1987) Progenesis as a principle in meiofauna evolution. J Nat Hist 21:843–854