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Thalassas 27 Thalassas, 27 (2): 169-192 An International Journal of Marine Sciences COMPARATIVE MORPHOLOGY OF THE MANTLE CAVITY ORGANS OF SHELLED SACOGLOSSA, WITH A DISCUSSION OF RELATIONSHIPS WITH OTHER HETEROBRANCHIA KATHE R. JENSEN(1) Key words: Shelled Sacoglossa, mantle complex, comparative morphology, Heterobranchia, Mollusca ABSTRACT osphradium is closely associated with shell adductor or cephalic/ pharyngeal retractor muscles, indicating The mantle cavity and pallial structures of that it is associated with the closure of incurrent water 18 species from 8 genera of shelled Sacoglossa flow to the mantle cavity. The genera Cylindrobulla, (Mollusca, Opisthobranchia) have been examined and Ascobulla and Volvatella are unique in having a compared with literature information about several long narrow section of the aperture between the taxa of Heterobranchia. Recent molecular studies anterior incurrent opening and the posterior excurrent have indicated an affiliation of the Sacoglossa and opening. This section forms a functional separation the Siphonariidae, a family of intertidal limpets of water currents and is lined by a row of glandular usually referred to basommatophoran Pulmonata. The bosses. In conclusion the Sacoglossa definitely stand gill of shelled Sacoglossa is unique within the taxa out from opisthobranch taxa, but the similarities with usually referred to Opisthobranchia by its attachment siphonariids are superficial and may be explained as to the surface of the kidney. Morphologically the homoplasies in response to similar environments. sacoglossan gill is similar to that of siphonariids, but In the future the fine structure of the kidney and the latter is located behind the kidney. The heart of pericardium of shelled Sacoglossa should be studied shelled Sacoglossa is almost completely detorted. in detail. This also differs from other basal heterobranch taxa. In the shelled Sacoglossa the inconspicuous INTRODUCTION Traditionally the Sacoglossa have been included as a monophyletic clade within the Opisthobranchia (Gosliner, 1981; Haszprunar, 1985a; Schmekel, 1985; (1) Zoological Museum (Natural History Museum of Denmark), Jensen, 1996a,b, 1997c; Mikkelsen 1996, 1998). Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark However, inclusion of molecular data has led to E-mail: [email protected] ambiguous relationships among the Euthyneura 169 Kathe R. Jensen Figure 1: A, Cylindrobulla sp. drawn by K.R. Jensen. B, Ascobulla fischeri from Jensen and Wells, 1990. C, Volvatella viridis from Jensen, 2003. D, Julia japonica redrawn from Kawaguti and Yamasu, 1962. E, Berthelinia darwini from Jensen, 1997a. F, Oxynoe azuropunctata, modified from Jensen, 1980. G, Roburnella wilsoni redrawn from Marcus, 1982. H, Lobiger souverbii redrawn from Marcus and Hughes, 1974 170 COMPARATIVE MORPHOLOGY OF THE MANTLE CAVITY ORGANS OF SHELLED SACOGLOSSA, WITH A DISCUSSION OF RELATIONSHIPS WITH OTHER HETEROBRANCHIA (=Opisthobranchia + Pulmonata) (Wägele et al., Based on morphological characters the 2003; Grande et al., 2004; Vonnemann et al., 2005). Volvatellidae, Julliidae and Oxynoidae form a The early molecular studies left the Sacoglossa monophyletic suborder, Oxynoacea (Jensen, 1996a), relatively unresolved between Opisthobranchia and and Cylindrobullidae is most likely sister group to Pulmonata (Thollesson, 1999; Dayrat et al., 2001), all remaining Sacoglossa (Jensen, 1996a,b), although but these studies included only one or two species some molecular studies include it in the Oxynoacea of Sacoglossa. Several new studies have indicated a (Händeler and Wägele, 2007; Maeda et al., 2010). closer relationship between the Sacoglossa and the Cylindrobulla and Ascobulla (Fig. 1A, B) have almost Siphonariidae, a family of limpets usually referred to identical cylindrical, thin, fragile shells with elastic the Pulmonata (Grande et al., 2008; Klussmann-Kolb periostracum and a sutural slit and keel (Jensen, 1989, et al., 2008; Dinapoli and Klussmann-Kolb, 2010; 1997c; Jensen and Wells, 1990; Mikkelsen, 1998). Jörger et al., 2010; Dinapoli et al., 2011; Dayrat et Volvatella (Fig. 1C) also has a thin, fragile shell with al., 2011). an elastic periostracum. Posteriorly the aperture is drawn out forming an exhalent spout. The foot is The mantle cavity and the pallial organs have relatively short, even in the extended state, and there been used to elucidate evolutionary theories for the are no parapodia or external pallial lobes to support Gastropoda for many years (reviewed by Lindberg the shell. In all of these three genera the head and and Ponder, 2001). The mantle structures of shelled foot may be completely withdrawn into the shell, and Sacoglossa are poorly studied. Most information the shell may be contracted by an anterior adductor is from descriptions of new species or anatomical muscle (Jensen, 1996a,b, 1997c). re-description of old species. The few existing comparative studies have been conducted from the The Juliidae are the bivalved sacoglossans. The point of view that the Sacoglossa were firmly lodged shell in these species has been divided into two in the Opisthobranchia (Gonor, 1961; Morton, 1988; “valves” of which the left bears the typical spirally Jensen, 1996b, 1997a,b). coiled protoconch and the right one covers the mantle fold. The “valves” are connected by an elastic The shelled Sacoglossa comprises the genera ligament. The animal can be completely retracted into Cylindrobulla, Ascobulla, Volvatella, Berthelinia, the shell (Baba, 1961). In Julia (Fig. 1D) the shell is Julia, Oxynoe, Lobiger and Roburnella (Fig. 1). thick and the protoconch is located far towards the The bivalved genera Tamanovalva, Edenttellina posterior end. Berthelinia (Fig. 1E) has thin shells and Midorigai are here considered synonyms of and the protoconch is located only slightly behind Berthelinia as no synapomorphic characters have been the middorsal point. Several fossil genera are known described to justify separate genera. The inclusion of from this family (Le Renard et al., 1996). Cylindrobulla in the Sacoglossa has been discussed previously (Jensen, 1989, 1996a,b; Mikkelsen, In the Oxynoidae the shell covers only the 1996, 1998), and the phylogenetic relationship of visceral mass and there is a long muscular tail and families and genera of shelled Sacoglossa remains lateral muscular parapodia. The head and anterior unclear (Händeler and Wägele, 2007; Händeler foot may be partly retracted into the shell, but et al., 2009; Maeda et al., 2010). Usually four the tail and parapodia cannot. The aperture of the families of shelled Sacoglossa are recognized: (1) shell is very wide. Oxynoe (Fig. 1F) has one pair Cylindrobullidae (Cylindrobulla), (2) Volvatellidae of parapodia, which can cover the shell almost (Volvatella, Ascobulla), (3) Juliidae (Julia, Berthelinia completely. Roburnella (Fig. 1G) has low parapodia, (Tamanovalva, Edenttellina, Midorigai)), (4) which carry two pairs of rolled extensions; these Oxynoidae (Oxynoe, Lobiger, Roburnella). may be folded across the shell or extended laterally. 171 Kathe R. Jensen Figure 2: Cylindrobulla sp. A, dorsal view after removal of shell. B, right anterior view, C, left side view, D, ventral view, E, mantle floor after removal of mantle fold. Arrow points to posteriormost point of aperture, i.e., where mantle edge turns forwards. F, ventral view of same, showing entrance to upper whorls. Legend: a – anus; add – shell adductor muscle; ar – adhesive ridge; cs – cephalic shield; dci – dorsal ciliated band; dci2 – dorsal ciliated band of penultimate whorl; dg – digestive gland; f – foot; fa – female aperture; fg – female glands; hy2 – second band of hypobranchial gland; i – intestine; ip – infrapallial lobe; k – apical keel of shell; me – mantle edge; g – gill; he – heart; hy – hypobranchial gland; sg – spawn groove; sh – shell; vci – ventral ciliated band. 172 COMPARATIVE MORPHOLOGY OF THE MANTLE CAVITY ORGANS OF SHELLED SACOGLOSSA, WITH A DISCUSSION OF RELATIONSHIPS WITH OTHER HETEROBRANCHIA Table 1: List of species and origin of material Species Locality/year Use Referencea Cylindrobulla phuketi Jensen, 1989 Phuket, Thailand 1990 Dissection Jensen, 1989, 1996b Cylindrobulla sp. Solomon Isl., 2007 Dissection present study Ascobulla ulla (Marcus and Marcus, Florida, 1978 Sections Marcus and Marcus, 1970) 1956; Jensen, 1996b; Mikkelsen, 1996, 1998 Ascobulla fischeri (Adams and Albany, WA, 1988 Dissection, Jensen and Wells, 1990; Angas, 1864) SEM Jensen, 1996b Ascobulla fragilis (Jeffreys, 1856) Mar Menor, Spain, 1993 Dissection present study Volvatella australis Jensen, 1997 Darwin, NT, 1993; Houtman Dissection Jensen, 1997a,b; present Abrolhos Islands, 1994 study Volvatella ventricosa Jensen and Albany, WA, 1988 SEM Jensen and Wells, 1990 Wells, 1990 Volvatella vigorouxi (Montrouzier, Singapore, 2006 Dissection Jensen, 2009 1861) Berthelinia babai (Burn, 1965) Victoria (Australia), 1988 SEM present study Berthelinia darwini Jensen, 1997 Darwin, NT, 1993; Houtman Dissection Jensen, 1997a,b; present Abrolhos Islands, 1994; study Cottesloe, WA, 1996 Berthelinia rottnesti Jensen, 1993 Rottnest Isl, WA 1991 Dissection Jensen, 1993 Julia cf. zebra Kawaguti, 1981 New Caledonia, 1993 Dissection present study Roburnella wilsoni (Tate, 1889) Rottnest Isl., WA 1991, 1996 Dissection Jensen, 1993; present study Lobiger souverbii Fischer, 1856 Barbados, 1977 Dissection Marcus, 1957; present study Oxynoe antillarum Mørch, 1863 St. Thomas, US Virgin Sections, Marcus and Marcus, Islands, 1982; Florida, 1992 dissection 1970;
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