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Redescription of the Meiofaunal Gastropod Parhedyle Cryptophthalma, with Focus on Nervous System and Sensory Organs

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Redescription of the Meiofaunal Gastropod Parhedyle Cryptophthalma, with Focus on Nervous System and Sensory Organs ©Zoologische Staatssammlung München/Verlag Friedrich Pfeil; download www.pfeil-verlag.de SPIXIANA 33 2 161–170 München, November 2010 ISSN 0341–8391 Redescription of the meiofaunal gastropod Parhedyle cryptophthalma, with focus on nervous system and sensory organs (Acochlidia, Panpulmonata) Katharina M. Jörger, Alen Kristof, Annette Klussmann-Kolb & Michael Schrödl Jörger, K. M., Kristof, A., Klussmann-Kolb, A. & Schrödl, M. 2010. Redescription of the meiofaunal gastropod Parhedyle cryptophthalma, with focus on nervous system and sensory organs (Acochlidia, Panpulmonata). Spixiana 33 (2): 161-170. Parhedyle cryptophthalma (Westheide & Wawra, 1974) is a poorly known meiofau- nal slug from the Mediterranean, inhabiting intertidal sands under direct wave impact. The present study is the first redescription of the acochlid P. cryptophthalma, confirming original results on general morphology, integumental spicules, and aberrant radula morphology by light and scanning electron microscopy. Our focus was on the central nervous system and sensory organs, using 3D reconstruction based on serial semi-thin sections and immunocytochemistry (staining of FMRFamide and Tyrosine Hydroxylase) in conjunction with confocal laser scan- ning microscopy. There is a mass of, yet undifferentiated, accessory ganglia ante- rior to the cerebral ganglia, typical for microhedylacean acochlidians. Apart from the common setting of ganglia (paired rhinophoral, cerebral, pedal, pleural, and buccal ganglia and three distinct ganglia on the visceral nerve cord), we found a putative osphradial ganglion for the first time in the microhedylacean clade. No osphradium, no Hancock’s organ and, in contrast to the original description, no pigmented eyes could be detected. Bundles of sensory cilia were found laterally on the head-foot complex and scattered cilia are present on the head appendages. FMRFamidergic immunoreactivity was detected in all cerebral ganglia but not in the accessory ganglia. Tyrosine Hydroxylase (TH) expression and aldehyde-in- duced fluorescence was observed in cerebral ganglia such as pedal ganglia, in labio tenctacular, rhinophoral, and pedal nerves and in single neurons in the ante- rior region of the foot sole. Central nervous and sensory features may greatly vary among acochlidians and other heterobranch taxa, and comprehensive comparative approaches are necessary to reveal their presence, function, homology, and evolu- tion. Katharina M. Jörger (corresponding author) & Michael Schrödl, Bavarian State Collection of Zoology, Münchhausenstr. 21, 81247 München, Germany, and De- partment Biology I of the Ludwig-Maximilians-Universität München, Großhader- ner Str. 2, 82152 Planegg-Martinsried, Germany; e-mail: [email protected]; [email protected] Alen Kristof, Research Group for Comparative Zoology, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark; e-mail: [email protected] Annette Klussmann-Kolb, Institute for Ecology, Evolution and Diversity, Jo- hann-Wolfgang-Goethe-University, Siesmayerstr. 70, 60054 Frankfurt am Main, Germany; e-mail: [email protected] 161 ©Zoologische Staatssammlung München/Verlag Friedrich Pfeil; download www.pfeil-verlag.de Introduction and/or cathecholaminergic parts of the nervous system have shown to provide phylogenetically Acochlidia are the most diverse and abundant group useful characters across different taxa (Dickinson of meiofaunal heterobranch gastropods. Inhabiting & Croll 2003, Croll & Dickinson 2004, Wanninger shallow subtidal sands worldwide some species 2009, Heuer et al. 2010, Kristof & Klussmann-Kolb may occur intertidally in protected places such as 2010, Worsaae & Rouse 2010). Moreover, spatial reef lagoons. In contrast, Parhedyle cryptophthalma distribution and immunoreactivity of neurites are (Westheide & Wawra, 1974) is known to occur on indicating their function (see Faller et al. 2008, and Mediterranean beaches with direct wave impact. references therein). Among Acochlidia Hochberg Despite recent advances in acochlidian morphology (2007) provided the first detailed information on and anatomy (Neusser et al. 2006, Neusser & Schrödl the chemistry of the nervous system in a species 2007, Jörger et al. 2008, Neusser et al. 2009a,b, Bren- of microhedylacean Asperspina. He revealed the zinger et al. in press), very little is still known about presence of an extensive serotoneric network in the the biology of these mainly marine mesopsammic central nervous system, with similarities to model slugs and the adaptation of the sensory and locomo- heterobranchs such as Aplysia, in the presence of tory system to their interstitial habitat. Being one serotoneric pericarya in cerebral and pedal ganglia of the smallest acochlids with an adult size of only and absence from pleural ganglia (Hochberg 2007). 1.6 mm the original description applying traditional Due to its minute body size Parhedyle cryptophthalma light microscopy lacks considerable detail, especially offers the possibility of immunocytochemical stud- regarding fine nervous structures. Moreover, a trend ies on whole-mount specimens for visualization by towards reduction within organ systems (“regressive confocal laser scanning microscopy (cLSM). evolution”), e. g. with aphallic males and reduced Here, we redescribe the nervous system and as- reproductive systems, is observed in the acochlid- sociated sensory structures of P. cryptophthalma by ian Microhedylacea clade (Swedmark 1959, 1968, 3D reconstruction from histological semi-thin serial Neusser et al. 2009b, Schrödl & Neusser 2010). The sections. To gain insights in the function of certain small amount of distinguishing characters paired nervous structures, this data is supplemented by the with a lack of morphological knowledge on some characterization of FMRFamidergic and chatecho- genera – in first place the genus Parhedyle – thus laminergic parts of the nervous system by means of still results in partially unresolved relationships immocytochemistry in conjunction with cLSM. The within Microhedylacea (for phylogeny, see Schrödl results are compared to other acochlidian nervous & Neusser 2010). systems and previous homology assumptions are The genus Parhedyle Thiele, 1931 was character- discussed. ized as a member of gonochoristic Microhedylidae having two pairs of highly mobile head tentacles and irregularly shaped spicule plates in the integument Material and methods (Wawra 1987). The type species Parhedyle tyrtowii Sampling (Kowalevsky, 1901) (as Hedyle) from the Black Sea was described to have clearly visible pigmented Specimens of Parhedyle cryptophthalma were recollected eyes and a symmetric radula with formula 2.1.2 at Arco Felice, near Naples, Italy, a locality that was by Kowalevsky (1901), while the Mediterranean reported in the original description by Westheide & P. cryptophthalma (as Microhedyle) has cryptic eyes Wawra (1974). Approximately 70 individuals were ex- and, uniquely among microhedylids, an asymmetric tracted from sand samples collected in the high interti- radula with a formula of 1.1.2 was found by light dal (wave zone) following the method described by Schrödl (2006). All specimens were anaesthetized with microscopical examination (Westheide & Wawra MgCl2 prior to fixation to prevent retraction. Specimens 1974). No details on central nervous or sensory were identified using light-microscopy and 10 individu- features are known. als were fixed in 75 % ethanol for radulae preparation. Traditionally, Acochlidia formed an order of the For histology and scanning electron microscopy (SEM) “Opisthobranchia” (see e.g. Dayrat & Tillier 2003, specimens were fixed in 4 % glutardialdehyde. Wägele & Klussmann-Kolb 2005), but recent multi- locus molecular data revealed pulmonate relation- Histology and 3D reconstruction ships (Klussmann-Kolb et al. 2008, Jörger et al. 2010). For serial semi-thin sectioning 20 glutardialdehyde- These recently proposed relationships question fixed specimens were embedded in Spurr’s low visco- traditional homology assumptions within Hetero- sity epoxy resin (Spurr 1969). Specimens were rinsed branchia and require re-evaluation of problematic three times in 0.2 M sodium cacodylate buffer (0.1 M character sets such as the nervous system. Investiga- NaCl and 0.35 M sucrose, pH 7.2), followed by post-fi- tions characterizing serotonergic, FMRFamidergic, xation in buffered 1 % OsO4 for 1.5 h in the dark. Sub- 162 ©Zoologische Staatssammlung München/Verlag Friedrich Pfeil; download www.pfeil-verlag.de Fig. 1. Light microscopy. A. External morphology of a living specimen. B. Oral tentacle and rhinophore, with scattered sensory cilia and circular bead-chain spicules (type 2). C. Typical J-shaped radula with ascending and descending limb. Abbreviations: c, cilia; lt, lateral tooth; ot, oral tentacle; r, radula; rh, rhinophore; rt, rhachidian tooth; sp1, plate-like spicules (type 1); sp2, circular bead-chain spicules; st, statocyst. sequently, specimens were decalcified in 1 % ascorbic Scanning electron microscopy (SEM) acid overnight and dehydrated in a graded acetone series. Four series of serial semi-thin sections (1.0-1.5 μm 10 entire specimens of Parhedyle cryptophthalma were thickness) were prepared using a diamond knife (Histo stepwise dehydrated in graded acetone series and crit- Jumbo, Diatome, Biel, Switzerland) and contact cement ical-point-dried in 100 % acetone in a Baltec CPD 030. on the lower cutting edge to form ribbons (Ruthenstei- After mounted on SEM stubs
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