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The Somatic Musculature of Bryceella Stylata (Milne, 1886) (Rotifera

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The Somatic Musculature of Bryceella Stylata (Milne, 1886) (Rotifera ARTICLE IN PRESS Zoologischer Anzeiger 248 (2009) 161–175 www.elsevier.de/jcz The somatic musculature of Bryceella stylata (Milne, 1886) (Rotifera: Proalidae) as revealed by confocal laser scanning microscopy with additional new data on its trophi and overall morphology E.F. Wiltsa,Ã, W.H. Ahlrichsa, P. Mart´ınez Arbizub aSystematics and Evolutionary Biology, Department of Biology and Environmental Sciences, Carl von Ossietzky University Oldenburg, 26111 Oldenburg, Germany bSenckenberg Research Institute, German Centre for Marine Biodiversity Research (DZMB), 26382 Wilhelmshaven, Germany Received 19 June 2009; received in revised form 10 August 2009; accepted 11 August 2009 Corresponding Editor: Sorensen Abstract The monogonont rotifer Bryceella stylata was investigated with light, electron and confocal laser scanning (CLSM) microscopy to provide detailed insights into its anatomy and new information for future phylogenetic analyses of the group. Results from CLSM and phalloidin staining revealed a total of six paired longitudinal muscles (musculi longitudinales I–VI) and eight circular muscles (musculi circulares I–VIII) as well a complex network of mostly fine visceral muscles. In comparison with other rotifer species that have been investigated so far, B. stylata shares the presence of the circular and longitudinal muscles: musculus longitudinalis ventralis, musculus longitudinalis lateralis inferior, musculus longitudinalis dorsalis, musculus longitudinalis capitis and musculus circumpedalis. However, the species lacks lateral and dorsolateral longitudinal muscles and some circular muscles (e.g., corona sphincter, musculus pars coronalis). With light and electron microscopy, we were able to document the precise number of pseudosegments and the arrangement of the chambers comprising the trophi elements. Furthermore, our observations revealed several new morphological characteristics, including a shield-like epidermal projection covering the dorsal antenna, an epidermal projection restricting the corona caudally and an unpaired hypopharynx with distinct shovel-like structures. & 2009 Elsevier GmbH. All rights reserved. Keywords: Rotifera; Proalidae; Morphology; Musculature; Confocal laser scanning microscopy 1. Introduction 2005b; Kotikova et al. 2006; Riemann et al. 2009). But these and other similar papers still investigate only a Our knowledge of the rotiferan musculature has small fraction of rotiferan taxa. A broader overview of improved recently in large measure due to the applica- the complex rotifer muscular system can only be tion of phalloidin-labelled dye combined with confocal achieved on the basis of adequate taxon sampling by laser scanning microscopy (CLSM) (e.g., Hochberg and including as many genera as possible. Data from further Litvaitis 2000; Sørensen et al. 2003; Sørensen 2005a, taxa are essential to accumulate more information about morphological variation in rotifer musculature and to ÃCorresponding author. retrace its evolution in detail (as emphasized by E-mail address: [email protected] (E.F. Wilts). Sørensen 2005a; Kotikova et al. 2001). 0044-5231/$ - see front matter & 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.jcz.2009.08.001 ARTICLE IN PRESS 162 E.F. Wilts et al. / Zoologischer Anzeiger 248 (2009) 161–175 The aim of this study is to contribute new data about For transmission electron microscopic (TEM) studies, rotiferan musculature in general and species of Proali- specimens were immobilized by exposing them to an dae in particular. Within Proalidae, detailed descriptions aqueous solution of 0.25% bupivacaine for 1 min and of the somatic musculature patterns exist for only a few subsequently fixing them with 1% OsO4 in 0.1 M species of Proales Gosse, 1886. As a first step towards sodium caodylate buffer at 8 1C. After fixation, speci- addressing this deficiency, we provide the first descrip- mens were dehydrated in an increasing acetone series at tion of the somatic musculature in a species of Bryceella 8 1C, subsequently embedded in Araldite hardened at using CLSM techniques. For small-sized species such as 60 1C for 72 h and ultrasectioned (75 nm) on a Reichert this, CLSM has proven itself to be a very potent ultracut followed by automatic staining with uranyl technique to visualize even the finest fibres that are acetate and lead citrate (Leica EM Stain). Examination otherwise difficult to observe in detail using conven- of the ultrathin sections was performed on a Zeiss 902 tional light microscopy. TEM at 80 kV. Although the small, dorsoventrally flattened species For CLSM, specimens were placed in a drop of of Bryceella are common in different aquatic and freshwater and relaxed in a 0.25% solution of bupiva- semiaquatic habitats (e.g., moors, the psammon of acid cine at 8 1C. The anaesthetised specimens were fixed for waters, ponds, mosses and leaf litter), our knowledge of 1 h in phosphate-buffered 4% paraformaldehyde and their morphology remains fragmentary. We found the rinsed in 0.1 M phosphate-buffered saline (PBS), and cosmopolitan rotifer Bryceella stylata (Milne, 1886)in then made permeable for staining by exposure to 0.1% mosses from a forest in Leer, North-west Germany and Triton X-100 buffered in 0.1 M PBS for 1 h. For seized the opportunity to reinvestigate its internal and staining, 2 mlof38mM methanolic TRITC-labelled external morphology using light and electron micro- phalloidin solution were added to 100 ml of Triton X- scopic techniques. Facing the lack of available appro- 100 buffered in 0.1 M PBS. Specimens were stained for priate morphological investigations across Proalidae 3 h and mounted in Citifluors on a cover slip; a total of and the necessity of a revision of this non-monophytetic five specimens were analyzed. The images were obtained group (see Wilts et al. 2009), our goal is to improve under wavelength of 488 nm using a Leica TCS SP 5 existing descriptions of this species and to present new confocal laser scanning microscope. We used ImageJ morphological details to support a subsequent phyloge- 1.37v and Leica LAS AF 1.7.0 for analysis of the image netic analysis that will hopefully clarify both the stacks. Line drawings were prepared using Adobe phylogenetic position of Bryceella and the phylogeny Photoshops CS2. of Proalidae in general. Our descriptions of the individual mastax jaw elements (trophi) and their relative positions follow the terminology previously introduced by Riemann et al. (2009), except that the terms dorsal manubrial 2. Material and methods chamber opening, median manubrial chamber opening and ventral manubrial chamber opening are replaced Moist mosses were collected during January 2007 by manubrium foramen dorsalis, manubrium foramen from a forest in Leer, North-west Germany medius and manubrium foramen ventralis in this (53115048.1400N, 7131054.4600E), transported to the la- study. boratory and subsequently cultured in plastic bags over several weeks. Single rotifer specimens were studied by both differential interference light microscopy (Leica DMLB) 3. Results and electron microscopy. Light microscopic images were taken with a digital camera (Olympus ColorView). 3.1. Diagnosis Isolated rotifer specimens were narcotized with bupiva- s caine (Bucain ) and fixed with a 4% OsO4 solution and Small, dorsoventrally flattened body; head region picric acid formaldehyde at 240 mOsm (after Melone narrow, trunk bulbous, foot slender; corona with two 1998). Specimens were dehydrated in a graded ethanol long lateral styli and forward directed cirri; rostrum oval series followed by critical-point drying. Dried specimens and broad; foot with three pseudosegments and were mounted on stubs and coated with gold. Trophi inwardly curving toes, consisting of three articulating were prepared under a stereomicroscope (Leica MZ125) joints; rami with six delicate spine-shaped projections following the procedure of De Smet (1998) but using anteriorly; distal subuncus with denticulate margin SDS/DTT (modified after Kleinow et al. 1990)as beneath the unci; fulcrum caudally slanted with ven- the dissolving agent. Specimens and trophi were studied trally directed hook; manubria broad, tapering distally; by scanning electron microscopy (SEM; Zeiss DSM multilayered hypopharynx with a paired shovel-like 940). structure anteriorly. ARTICLE IN PRESS E.F. Wilts et al. / Zoologischer Anzeiger 248 (2009) 161–175 163 Fig. 1. General body organization of Bryceella stylata. (A) Specimen from dorsal side; (B) specimen in lateral view; (C) mastax hard parts (trophi) in dorsal view. ds=distal subuncus, fu=fulcrum, hyp=hypopharynx, ma=manubrium, ra=ramus, un=uncus. 3.2. General body organization of parthenogenetic (Fig. 3B). The most anterior pseudosegment presents a females large, semicircular to oval rostrum (Fig. 2B) and is followed by two additional short and rectangular 3.2.1. Habitus pseudosegments (Figs. 1B and 3C, D) in which the B. stylata has a hyaline and weakly stiffened, trophi (Fig. 2A, C, D) are located. A dorsal antenna dorsoventrally flattened body with a narrow head, a inserts at the intersection of the first and second head bulbous trunk and a slender foot (Figs. 1A and 2A). pseudosegments (Fig. 3D). The third head pseudoseg- The whole body is divided into three distinct regions: ment, the so-called neck pseudosegment, adjoins the head with neck, trunk and foot with toes (Figs. 1A, trunk. The planar corona is limited to the ventral head Band3A, B). The surface of the epidermis is region and extends ventrally from the most anterior smooth. TEM
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