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Fine Morphology of the Jaw Apparatus of Puncturella Noachina (Fissurellidae, Vetigastropoda)

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Fine Morphology of the Jaw Apparatus of Puncturella Noachina (Fissurellidae, Vetigastropoda) JOURNAL OF MORPHOLOGY 00:00–00 (2014) Fine Morphology of the Jaw Apparatus of Puncturella noachina (Fissurellidae, Vetigastropoda) Elena Vortsepneva,1* Dmitry Ivanov,2 Gunter€ Purschke,3 and Alexander Tzetlin1 1Department of Invertebrate Zoology, Moscow State University, 119234 Moscow, Russia and White Sea Biological Station, Russia 2Zoological Museum, Moscow State University, Bolshaya Nikitskaya Str. 6, 225009 Moscow, Russia 3Zoologie, Fachbereich Biologie/Chemie, Universitat€ Osnabruck,€ 49069 Osnabruck,€ Germany ABSTRACT Jaws of various kinds occur in virtually Wingatrand, 1959), Scaphopoda (Schaefer and Hasz- all groups of Mollusca, except for Polyplacophora and prunar, 1996), and Gastropoda (Patellogastropoda, Bivalvia. Molluscan jaws are formed by the buccal epi- opisthobranch Euthyneura), the second in Gastrop- thelium and either constitute a single plate, a paired oda (Opistobranchia), Aplacophora (Ivanov and formation or a serial structure. Buccal ectodermal Starobogatov, 1990), and Cephalopoda (Boletzky, structures in gastropods are rather different. They can be nonrenewable or having final growth, like the hooks 2007), and the third is restricted to Gastropoda in Clione (Gastropoda, Gymnosomata). In this case, (opisthobranch Euthyneura; Barker and Efford, they are formed by a single cell. Conversely, they can 2002). In all molluscs, the jaw lies in the buccal cav- be renewable during the entire life span and in this ity and occupies a lateral, dorsal, or dorso-lateral case they are formed by a set of cells, like the forma- position. The lower jaw of Cephalopoda takes a ven- tion of the radula. The fine structure of the jaws was tral position and is regarded as not being homolo- studied in the gastropod Puncturella noachina. The jaw gous to the jaws of other molluscs (Boletzky, 2007). is situated in the buccal cavity and consists of paired Thus, the highest diversity in jaw morphology elongated cuticular plates. On the anterior edge of each occurs in gastropods possessing single dorsal jaw cuticular plate there are numerous longitudinally ori- plates (Patellogastropoda, occulinida), paired jaw ented rodlets disposed over the entire jaw surface and immersed into a cuticular matrix. The jaw can be plates situated on the dorso-ventral side (Nudi- divided into four zones situated successively toward the pleura), and serial jaw plates on the dorsal side of anterior edge: 1) the posterior area: the zone of forma- the buccal cavity (opisthobranch Euthyneura). tion of the thick cuticle covering the entire jaw and The presence of two separate symmetrical forming the electron-dense outer layer of the jaw plate; (paired) jaw plates in opisthobranch Euthyneura 2) the zone of rodlet formation; 3) the zone of rodlet (Cephalaspidea, Thecosomata, Anaspidea, almost arrangement; and 4) the anterior zone: the free scrap- all Nudipleura) is suggested to be plesiomorphic ing edge of the plate, or the erosion zone. In the gen- for Euthyneura, whereas the absence of jaws (Cri- eral pattern of jaw formation, Puncturella noachina mora, many Cryptobranchia, e.g., Doris, Archido- resembles Testudinalia tessulata (Patellogastropoda) ris, Austrodoris, and Sclerodoris, Dendrodorididae, studied previously. The basis of the jaw is a cuticular plate formed by the activity of the strongly developed Phyllidiidae) is regarded as apomorphic (Gosliner, microvillar apparatus of the gnathoepithelium. How- 1994; Wagele and Willan, 2000). Two separated ever, the mechanism of renewal of the jaw anterior plates consisting of rod-like structures also occur part in P. noachina is much more complex as its scrap- in rhipidoglossate Gastropoda (Haszprunar, ing edge consists not just of a thick cuticular matrix rather than of a system of denticles being the projec- ting endings of rodlets. J. Morphol. 000:000–000, 2014. VC 2014 Wiley Periodicals, Inc. Contract grant sponsor: The Russian Foundation; Grant num- bers: N-3-119-10; 12-04-32293; Contract grant sponsor: The KEY WORDS: Fissurellidae; Gastropoda; Puncturella Ostpartnerschaften-Programm des Deutschen Akademischen noachina; ultrastructure of jaws Austauschdienstes. *Correspondence to: Elena Vortsepneva; Department of Inverte- brate Zoology, Moscow State University, 119234 Moscow, Russia and White Sea Biological Station, Russia. INTRODUCTION E-mail: [email protected] Jaws of various kinds occur in virtually all groups of Mollusca except for two taxa: Polyplacophora and Received 2 October 2013; Revised 14 January 2014; Bivalvia. Molluscan jaws are formed by the buccal Accepted 19 January 2014. epithelium and either constitute a single plate, a Published online 00 Month 2014 in paired formation or a serial structure. The first type Wiley Online Library (wileyonlinelibrary.com). of jaw is found in Monoplacophora (Lemche and DOI 10.1002/jmor.20259 VC 2014 WILEY PERIODICALS, INC. 2 E. VORTSEPNEVA ET AL. 1988a,b), many Caenogastropoda (Strong, 2003), C; 2A,B; 3A,B). The buccal cavity is not very vast. and many basal Heterobranchia (Ponder, 1991). In In the retracted state the radula slightly protrudes Pyramidelloidea (Euthyneura) they are highly into the buccal cavity. The radula fills the most modified to form stylets (Ponder, 1991). part of the buccal cavity in relaxed specimens Despite the availability of rather complete infor- (Fig. 2A; 3A,B). The paired jaw is situated opposite mation about the general morphology of the jaws to the radula. In the retracted state of the radula in various gastropod groups, there are only few its parts are somewhat drawn apart (Fig. 1D–I; investigations on both, the fine structure of the 2A), while in the protracted position they are con- jaws (Hughes, 1979) and peculiarities of the for- nected and form a single surface (Fig. 2C). The mation and growth of the jaws (Thompson, 1962; oesophagus originates from the buccal cavity pos- Lufty and Demian, 1967). This makes the compar- terior dorsally. In the contracted state of the ani- ison of these structures among different molluscan mal it forms a loop and fills the anterior part of groups virtually impossible. Therefore, Vortsep- the head so that the cerebral commissure is fixed neva et al. (2013) and Vortsepneva and Tzetlin between the oesophagus and the roof of the buccal (2013) have obtained new data on the structure cavity (Fig. 1D–F). In the protracted position of and on the growth pattern of the jaws in some spe- the radula, the oesophagus does not form a loop in cies of Patellogastropoda and Nudipleura. This the head (Fig. 2A; 3A). A pair of small salivary work continues this series of publications and is glands open into the buccal cavity laterally; they devoted to the fine structure of the jaws in a rep- lack ducts (Fig. 1A–C, sg). resentative of Vetigastropoda. General and Fine Morphology of the Jaw MATERIAL AND METHODS Each of the two paired jaw plates has an elon- Material gated shape (up to 310 lm in length), narrowed During the summer months of 2007–2009, about 25 speci- posteriorly (up to 100 lm in width) and expanded mens of Puncturella noachina Linnaeus, 1771 [subtidal, about anteriorly (up to 220 lm in width). Numerous lon- 30 m deep (66 33’ 1824’’ N, 33 08’0874’’E)] were sampled near gitudinally oriented rodlets lie inside the anterior the biological station of the Moscow State University, Kanda- laksha Bay, White Sea, Russia. Ten fixed specimens of P. noa- expanded part of the jaw plate. They are 70 lm china were studied using semithin and ultrathin sectioning, long on average (Fig. 2C–F). Each jaw plate con- with the aid of transmission electron microscopy (TEM) and tains about 1,000 rodlets. The space between the scanning electron microscopy (SEM). The specimens were rodlets is filled by a less electron-dense matrix relaxed in 7% MgCl2 for 1 h before fixation. with a few electron dense rounded inclusions up to Specimens for electron microscopy studies were fixed in 2.5% glutaraldehyde in 0.1 mol l21 phosphate buffer (pH 7.2–7.4). 10 lm in diameter. The matrix is eroded on the After rinsing in the same buffer, specimens were postfixed with anterior edge of the jaw, and the rodlets protrude buffered 1% osmium tetroxide, dehydrated in a graded ethanol from the jaw plate (by 65 lm on average) and series, and then transferred to acetone. For TEM, specimens form the jagged scraping edge of the jaw (Fig. 2C; were embedded in Epon 812 resin. Semithin and ultrathin sec- 3D). The plates are almost entirely attached to the tions were made on Dupont MT 5000 (Sorvall, Newtown, USA) and Leica EM UC 6 (Solms, Germany) ultramicrotomes. Four epithelium and only have free anterior and outer longitudinal series and three transversal series of semithin and lateral margins (Fig. 3D,E). ultrathin sections were made for studying the jaws in P. noa- The jaw can be divided into four zones according china. Semithin sections were stained with 1% toluidine blue- to the peculiarities of the ultrastructure of the 1 1% methylene green on the 1% sodium tetraborate. Ultrathin sections were stained with lead citrate (15 min) and uranylace- cuticle and its underlying cells, called gnatho- tate (1%, 40 min, 35) and examined with a Jeol JEM 1011 blasts. These zones are sequentially situated ante- transmission electron microscope, Institute for Biology of riorwards: 1) the posteriormost zone, that is, the Inland Waters of the Russian Academy of Sciences, and with a area of formation of the thick cuticle covering the Zeiss EM 902A (at the University of Osnabrueck, Germany). entire jaw and forming the electron-dense outer For SEM, fragments of dissected bodies were dried using the layer of the plate; 2) the zone of rodlet formation; critical point method with CO2, mounted on aluminium stubs, sputter coated with platinum–palladium, and examined with a 3) the zone of fully formed rodlets becoming HITACHI 400A SEM. arranged longitudinally and in several layers; 4) Three-dimensional reconstructions were made from series of the anterior free scraping edge of the plate, or the semithin sections by the method described by Ruthensteiner and zone of erosion (Fig.
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