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'Cejkaian Tubules' in the Posterior Midgut of Terrestrial Enchytraeidae (Oligochaeta)

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'Cejkaian Tubules' in the Posterior Midgut of Terrestrial Enchytraeidae (Oligochaeta) 85 (2) · August 2013 pp. 113–122 ‘Cejkaian tubules’ in the posterior midgut of terrestrial Enchytraeidae (Oligochaeta) Rüdiger M. Schmelz1,2,* and Rut Collado2 1 ECT Oekotoxikologie GmbH, Böttgerstrasse 2–14, 65439 Flörsheim am Main, Germany 2 Universidad de A Coruña, Fac. Ciencias, Dep. Biología Animal, Biol. Vegetal, y Ecología, Rua da Fraga 10, 15008 A Coruña, Spain * Corresponding author, e-mail: [email protected] Received 29 May 2013 | Accepted 2 July 2013 Published online at www.soil-organisms.de 1 August 2013 | Printed version 15 August 2013 Abstract More than one hundred years ago, Bohumil Čejka described peculiar elongate tubules in the posterior region of the intestine of Hepatogaster birulae, a new terrestrial enchytraeid species collected in North-East Siberia. The tubules have no cilia but a proper epithelium and they run parallel to the longitudinal axis of the intestine over several segments, inside the intestinal epithelium but in close contact with the blood sinus. The tubules end blindly anteriorly and with a porus to the intestinal lumen posteriorly. The number of tubules increases from posterior to anterior due to bifurcations, and their diameter decreases. Čejka hypothesized that these tubules are glands that provide secretions for the final process of digestion or that aid in the egestion of faeces. He found them only in one species, Hepatogaster birulae, which was later synonymized with Henlea ochracea. In recent years we screened a large number of terrestrial enchytraeids in vivo and found these peculiar tubules in two further species of Henlea, in one species of Oconnorella and in thirteen species of Fridericia. The pores of these tubules are always located near the transition from midgut to hindgut. The tubules vary among species in extent and branching pattern, and several types can be distinguished. We suggest naming the structures ‘Cejkaian tubules’ in honour and memory of the finder, whose last publication dates from 1914. ‘Cejkaian tubules’ were not found in every species of Henlea and Fridericia, and they seem to be absent in other genera, but techniques other than in vivo light microscopy are required to confirm their absence with certainty. As to their function, we hypothesize the opposite of Čejka, not secretion but resorption, possibly of water, similar to the colon in tetrapod vertebrates. Keywords Intestine | invertebrates | Clitellata | Annelida | live investigation 1. Introduction better knowledge of the different gut regions should increase our understanding of the process of digestion, Knowledge and understanding of the digestive tract which includes several steps such as physical and in enchytraeids is important for at least four reasons: chemical diminution of particles, ingestion of nutrients 1) In contrast to other microdrile oligochaete taxa, and absorption of water. Different gut regions may be differentiations of the intestine in Enchytraeidae are specialized for specific functions, however the simple highly diverse and are used to recognize genera and question ‘what happens where’ in the gut of enchytraeids species (Nielsen & Christensen 1959, Kasprzak 1984, has rarely been addressed (but see Gelder 1984, Mothes- Schmelz & Collado 2010). 2) The pattern of characters Wagner et al. 1996, Reichert et al. 1996). 4) Finally, associated with the gut may be useful for phylogenetic enchytraeids feed on the medium in which they live, reconstruction, for understanding evolutionary pathways like many other oligochaetes, and alter it during passage or for interpreting differences in the autecology and through the gut (Didden 1993, Haimi & Siira-Pietikäinen lifestyle of the species. 3) In more general terms, a 2003). Therefore knowledge of gut structure and function © Senckenberg Museum of Natural History Görlitz · 2013 ISSN 1864-6417 SO85(2).indb 1 31.07.2013 09:31:44 114 Rüdiger M. Schmelz & Rut Collado should help to understand the contribution of this group of size and position are taxon-specific (Schmelz & Collado animals to the formation, maintenance or alteration of the 2010). Cell modifications include the so-called ‘chylus ecosystems of which they are part. cells’ (Michaelsen 1886, Schmelz 2003) with intracellular The digestive tract of enchytraeids follows the general canals, present only in Fridericia. oligochaete model of a ‘tube within a tube’, running Only few morphological or histological differentiations straight or with slight sinuosities through the body have been described in the posterior gut region. A field from the anterior mouth to the posterior anus (Fig. 1). of ventrally inflated and vesicular gut epithelium, named In cross-section it consists of the gut epithelium proper, ‘pars tumida’ in Schmelz et al. (2008) was found in surrounding blood sinus and an envelope of mesodermal terrestrial taxa (Rota 1995, Rota & Healy 1999, Schmelz tissue, differentiated into musculature and chloragocytes, et al. 2008, 2011, Schmelz & Collado 2013) and appears to the latter in contact with the coelomic fluid. A dorsal be part of the standard equipment of the enchytraeid gut. blood vessel rises from the blood sinus in the anterior Rota et al. (2007) distinguished a caudal gut dilatation in body region and projects anteriad to the head region some species of the exclusively marine genus Grania and (Fig. 1). In developmental terms, there are three gut termed it ‘rectal ampulla’. Gelder (1984) documented a regions, the ectodermal foregut, the endodermal midgut gut region-specific presence of various digestive enzymes and the ectodermal hindgut, accordant with the ground in Lumbricillus lineatus (Müller) and Mothes-Wagner plan of annelids (Westheide & Rieger 2006). In functional et al. (1996) described region-specific ultrastructural terms, five gut regions are distinguished in enchytraeids: differentiations of the intestinal epithelium; both studies buccal cavity, pharynx, oesophagus, intestine and rectum include the posterior gut region. (Gelder 1984, Mothes-Wagner et al. 1996). Here we describe one more differentiation of the intestinal The greatest variety of light-microscopically distingu- epithelium. Its discovery goes back to Bohumil Čejka ishable differentiations is found in the posterior foregut (1910). More than one hundred years ago, he described and the anterior midgut, a region equivalent to pharynx two new enchytraeid species collected in North-East and oesophagus, and the variations comprise three types Siberia and ascribed them to a new genus, Hepatogaster. of outgrowth structures and several cellular modifications. According to Čejka (1910), one of these species, named 1) Pharyngeal glands are strongly developed in all H. birulae, has peculiar elongate tubules in the posterior enchytraeids, but are of varying shape and arrangement region of the intestine (Fig. 2). The tubules have no cilia but among taxa. These solid glands form a functional unit a proper epithelium and they run parallel to the longitudinal together with the dorsal pharyngeal pad, the organ of food axis of the intestine over several segments, inside the uptake in most oligochaetes (Stephenson 1930, Jamieson intestinal epithelium but in close contact with the blood 1981, Purschke 2003). According to Ude (1977), all sinus. The tubules end blindly anteriorly, and a posterior digestive enzymes are produced here. 2) Oesophageal porus connects with intestinal lumen. The number of tubules appendages are tube- or sponge-like outfoldings of the gut increases from posterior to anterior due to bifurcations, and epithelium in segments III to VII, and they differ among their diameter decreases. Čejka hypothesized that these taxa in presence/absence, shape, size, histology and mode tubules are glands that provide secretions for the final of attachment to the gut (Schmelz & Westheide 2000). process of digestion or that aid in the egestion of faeces. He 3) Intestinal diverticula are sac- or pouch-like outgrowths states explicitly that these tubules are absent in the second of the intestine located more posteriorly, usually in species, H. sibiricus, but according to a figure (see Fig. 2D), segments VI to VIII. Again presence/absence, shape, they seem to be present also in this species. pp pg dv bw ie il pt ct foregut midgut hindgut buccal cavity oesophagus intestine rectum + pharynx Figure 1. Gut regions in enchytraeids, a generalized scheme, lateral view, mouth to the left. Thick lines – cuticle, bw – body wall with chaetae (lateral chaetae omitted), ct – Cejkaian tubules, dv – dorsal blood vessel, ie – intestinal epithelium, il – intestinal lumen, pg – pharyngeal gland, pp – pharyngeal pad, pt – midgut pars tumida. SOIL ORGANISMS 85 (2) 2013 SO85(2).indb 2 31.07.2013 09:31:45 Cejkaian tubules in Enchytraeidae 115 In the subsequent literature these tubules found little In recent years we screened a large number of terrestrial interest and were mentioned only as possible distinguishing enchytraeids in vivo, and we found these peculiar tubules characters between the genera Hepatogaster and Henlea in two further species of Henlea, in one species of (Welch 1920, Stephenson 1922, 1930), an option rejected Oconnorella and in thirteen species of Fridericia. We also by Černosvitov (1931). Later the genus was united with found them to be species-constant and morphologically Henlea (Nielsen & Christensen 1959) and the species was diverse among species. A short note on these tubules in united with Henlea ochracea (Eisen, 1878) (Nurminen Fridericia was published previously (Schmelz 2003: 43). 1973) - hence the nomenclaturally
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