Zoomorphology (1997) 117:135–145
© Springer-Verlag 1997
O R I G I NA L A RT I C L E
&roles:Holger Herlyn · Ulrich Ehlers
Ultrastructure and function of the pharynx of Gnathostomula paradoxa (Gnathostomulida)
&misc:Accepted: 4 April 1997
&p.1:Abstract The pharynx of Gnathostomula paradoxa consists of the partly syncytial pharyngeal musculature, a pharyngeal epithelium, myoepitheliocytes, receptors, nerves, and three solid parts, called the jugum, the basal plate, and the jaw. Extended non-contractile regions of both pharyngeal and body wall musculature form the socalled parenchymatous tissue between the digestive tract and the body wall. The pharyngeal epithelium mediates the force from the pharyngeal musculature to the solid parts. The basal plate and jaw contain longitudinal cuticular rods which are elastic antagonists of the musculature. There is no buccal ganglion in G. paradoxa. The study supports the monophyly of the Gnathostomulida and Gnathifera.&bdy:
A. Introduction Gnathostomulida have been known since the investigation of the marine interstitium by Remane in the 1920s (see Ax 1956). Gnathostomula paradoxa Ax, 1956 and Gnathostomaria lutheri Ax, 1956 were the first two species to be described. Today round about 100 species are known (Sterrer 1996). While the monophyly of Gnathostomulida was never disputed, their sister group remained questionable for a long time. Ax (1984, 1995) regarded the Plathelminthes as the sister group and he grouped both taxa togther as the Plathelminthomorpha. However, Reisinger (1961) discussed the Rotifera as a potential sister group. This hypothesis was supported by ultrastructural data on the mastax of the Rotifera (Koehler and Hayes 1969a, b) and by unpublished findings of Lammert on the jaw of the Gnasthostomulida (see Rieger and Tyler 1995). One aim of the present study is to describe the pharyngeal ultrastructure of G. This paper is dedicated to Professor Dr. Peter Ax, Göttingen, on the occasion of his 70th birthday H. Herlyn (✉) · U. Ehlers II. Zoologisches Institut und Museum der Universität Göttingen, Berliner Strasse 28, D-37073 Göttingen, Germany Fax: 0049-511-5448; e-mail:
[email protected]&/fn-block:
paradoxa. Gnathostomulida and Syndermata (=Rotifera+Seison+Acanthocephala) were grouped together as Gnathifera Ahlrichs, 1995 (Ahlrichs 1995; see Rieger and Tyler 1995). Recently Ahlrichs (1997) also included a new unnamed taxon (“new group A”) in the Gnathifera. Ahlrichs (1995) and Ehlers et al. (1996) discussed the phylogenetic position of the Gnathifera within the Bilateria. To test the validity of the Gnathifera is another aim of our study.
B. Materials and methods Specimens of G. paradoxa were collected in April 1995 in the tidal flats of the so-called Königshafen off List/Sylt (Germany). Sediment from the burrows of Arenicola marina (Linné, 1758) was placed in Kautex bottles and taken to the laboratory of the Biologische Anstalt Helgoland. In the laboratory, the meiofauna was extracted by the seawater-ice method (Pfannkuche and Thiel 1988). The concentrated samples were sorted under 50× magnification. The specimens so stunned were prefixed with ruthenium redtinted 2.5% glutaraldehyde in 0.1 M sodium cacodylate buffer (pH 7.2) for 1 h at 4° C. Rinsing in 0.1 M sodium cadocylate buffer was followed by postfixation in 1% osmium tetroxide, in the same buffer, for 1 h at 4° C. The specimens were dehydrated in a graded acetone series and embedded in Araldite (intermedium: polypropylene). Ultrathin silver-interfering sections (ca. 70 nm) were cut (Reichert Ultracut-II, Diatome diamond knife). The sections were put on Formvar-coated, one-slit grids. After automatic double staining with uranyl acetate and lead citrate (two times, LKB Ultrastainer) the sections were viewed (Zeiss EM 900, at 50 kV). Section series from two cross-sectioned specimens and from one longitudinally sectioned specimen were investigated. Results (microphotographs and drawings) were taken from one cross-sectioned specimen.
C. Results The digestive tract of G. paradoxa comprises the ventral mouth opening, the pharynx, and the blind intestine. The pharynx consists of musculature, an epithelium, myoepitheliocytes, receptors, nerves, and solid parts (the jugum, basal plate and jaw).
136 Fig. 1A, B Position of the cross-sections depicted in Figs. 2–7. A Schematic reconstruction of the basal plate of G. paradoxa on the basis of serial sections, dorsal view. B Schematic reconstruction of the jaw of G. paradoxa on the basis of serial sections, dorsal view. bpd basal plate disc, ca cauda, dl dorsal lamella, jh jaw half, rt rostral tooth row, rw rostral wing, sy symphysis, tr toothrows, vl ventral lamella&ig.c:/f
I. Pharyngeal musculature Two unpaired and unbranched myocytes, 2 unpaired and branched myocytes, 8 paired and branched myocytes, and two paired and highly branched myosyncytia form the pharyngeal musculature proximal to the basal lamina. These 12 myocytes and two myosyncytia consist of non-contractile and contractile regions. The extended non-contractile regions contain plenty of sarcoplasm, the nucleus, a diplosome, rough endoplasmic reticulum, free ribosomes, the Golgi apparatus, and mitochondria (Figs. 2, 5, 6: bl, cr, ncr, rER). The contractile regions show cross-striated myofibrils pulling in different directions and little sarcoplasm. The cross-striation of the myofibrils is caused by bands of isolated z-dots located between the sarcomeres. The non-contractile regions of myocytes and myosyncytia are not entirely surrounded by an extracellular matrix (Figs. 2–6: ecm, zd). The contractile regions from the muscle capsule (Figs. 2–6: mca), the paired lateral muscle pouches (Fig. 5: lp), and the unpaired caudal muscle pouch (Fig. 6 cp). The muscle capsule is 58 µm long, up to 34 µm wide and up to 30 µm high. The non-contractile regions form two dorsolateral tissue lobes and one ventral tissue lobe which exceed the muscle rostrally and caudally respectively. The tissue lobes are not distinguishable from the surrounding non-contractile tissue at both the light and electron microscopic levels (Figs. 2, 4, 5: dtl, vtl). II. Pharyngeal epithelium The unilayered cellular epithelium lies distally to the basal lamina. The apical cytoplasm has free ribosomes, a diplosome, and different vesicles. The basal cytoplasm shows free ribosomes, the nucleus, much rough endo-
plasmic reticulum, the Golgi apparatus, and mitochondria. The epithelium has no ciliation and is differentiated into two types: a secretion epithelium with many vesicles and long microvilli covered by a glycocalyx (Figs. 2–6, bl, gm, rER, ve), and a force-mediating epithelium characterized by tonofilaments running from desmosomes and hemidesmosomes to the solid parts (Figs. 2–5, 7A: ds, tf, hd). III. Pharyngeal myoepitheliocytes One pair of myoepitheliocytes is embedded in the pharnygeal epithelium. These cells (length about 22 µm) run from the transition between the mouth cavity and esophagus to the caudal end of the caudal muscle pouch. The apical cell membrane shows microvilli covered by a glycocalyx. A diplosome and some vesicles exist in the apical cytoplasm. The basal cytoplasm includes the nucleus and mitochondria. Contractile filaments run from the apical to the basal cell membrane. Bands of isolated zdots located between the sarcomeres cause a cross-striation of the myofibris. Anteriorly, both myoepitheliocytes appear in cross-sections as an erected U (Figs. 3–5: cp, e, gm, me, mc, pe, ve, zd). IV. Pharyngeal solid parts G. paradoxa has three separate pharyngeal solid parts, the jugum, the basal plate, and the jaw. The solid parts consist of different types, turning at the margins into a glycocalyx. In the following, the jugum, situated at the anterior rim of the mouth opening, will not be considered. The basal plate and the jaw share vertical rows of longitudinal cuticular rods (diameter up to 0.4 µm) in their construction. The cuticular rods consist of an elec-
137 Fig. 2 Cross-section of the pharnynx of G. paradoxa. Noncontractile regions (ncr) of the pharyngeal musculature form the dorsolateral tissue lobes (dtl). The pharyngeal epithelium (pe) includes much rough endoplasmic reticulum (rER) and many vesicles (ve). The basal plate, consisting of rostral wings (rw) and rostral tooth row (rt), separates the mouth cavity (mc) from the ventral mouth opening (mo). Both jaw halves (jh) show two tooth rows (tr). bl basal lamina, cr contractile regions, ds desmosomes, ecm extracellular matrix, gm glycocalyx-covered microvilli, hs hemidesmosomes, mca muscle capsule, mf myofibrils, zd z-dots&ig.c:/f
tron-dense core containing cuticular material and a glycocalyx surrounded by an electron-lucent halo also of cuticular material. The halo is interrupted by pores and slits. The cuticular material and the glycocalyx of the core touch the cuticular material and glycocalyx outside the cuticular rods along these pores and slits (Figs. 3, 4, 7A, B: cd, dc, gc, lh). The basal plate is divided anteriorposteriorly into the following components (lengths in parentheses) (Fig. 1A): paired rostral wings (ca. 9 µm), a rostral tooth row located between the rostral wings (ca. 7 µm) and a basal plate disc (ca. 12 µm). In total the basal plate mea-
sures ca. 20 µm in length, maximally ca. 24 µm in width measured along the rostral wings, and maximally ca. 4 µm in height measured along the basal plate disc. Anteriorly the basal plate separates the mouth cavity from the mouth opening (Fig. 2). Posteriorly it lies on the ventral pharyngeal epithelium. Altogether, 14 cuticular rods are arranged in paired vertical arcs at the median margins of the rostral wings (Fig. 7B: bpd, cd, mc, mo, pe, rt, rw). The longitudinal jaw has a horizontal resting position within the mouth cavity. It consists, from anterior to posterior, of the following parts (lengths in parentheses)
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Fig. 3 Cross-section of the pharynx of G. paradoxa. Beginning of the esophagus (e) and of myoepitheliocytes (me). Division of the jaw halves into inner walls (iw), dorsal lamellae (dl), and ventral lamellae (vl). Note the distinct tonofilaments (tf) running from desmosomes (ds) to hemidesmosomes (hs). bl basal lamina, cr contractile regions, ecm extracellular matrix, gc glycocalyx, gm glycocalyx-covered microvilli, ir inner row, mc mouth cavity, mca muscle capsule, mf myofibrils, pe pharyngeal epithelium, rER rough endoplasmic reticulum, ve vesicles, zd z-dots&ig.c:/f
(Fig. 1B): paired jaw halves (ca. 24 µm) armed with three horizontal tooth rows (ca. 9 µm), an unpaired symphysis (ca. 9 µm) resulting from the joining of the inner walls of the jaw halves, paired dorsal (ca. 1 µm) and paired ventral lamellae (ca. 8 µm) resulting from the dorsal and ventral parts of the jaw halves, and an unpaired cauda (ca. 11 µm) following the symphysis. The symphysis and cauda overlap for ca. 2 µm. Altogether the jaw measures ca. 34 µm in length, maximally ca. 8 µm in width measured along the cauda, and maximally ca. 10 µm in height measured along the jaw halves (Figs. 2–5: ca, dl, iw, jh, mc, sy, tr, vl). In all, the jaw contains 81 cuticular rods arranged in five vertical rows. The paired
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Fig. 4 Cross-section of the pharynx of G. paradoxa. Myofibrils (mf) of the pharyngeal musculature insert broughtly in the symphysis (sy). Both myoepitheliocytes (me) appear as an erected U. The paired inner rows (ir), the paired outer rows (or), and the unpaired median row (mr) are visible within the symphysis. bl basal lamina, ca cauda, cr contractile regions, ds desmosomes, e esophagus, ecm extracellular matrix, gm glycocalyx-covered microvilli, hs hemidesmosomes, mca muscle capsule, ncr non-contractile regions, pe pharyngeal epithelium, rER rough endoplasmic reticulum, tf tonofilaments, ve vesicles, vl ventral lamella, vtl ventral tissue lobe, zd z-dots&ig.c:/f
inner rows (ca. 18 µm) start the tooth rows of the jaw halves and extend into the symphysis. They consist of 60 cuticular rods and reach maximally ca. 5 µm in height. The outer rows (ca. 2 µm) are also paired, contain 18 cuticular rods, and reach maximally ca. 2 µm in height. They run through the symphysis. The unpaired median row (ca. 5 µm) with a maximal height of ca. 1 µm also runs through the symphysis. It consists of 3 cuticular rods. The longest cuticular rods are located halfway between the dorsal and ventral edge of every row. Dorsally and ventrally to these the cuticular rods get shorter.
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Fig. 5 Cross-section of the pharynx of G. paradoxa. Extended non-contractile regions (ncr) of the pharyngeal musculature are visible within the contractile regions (cr). The lateral muscle pouches (lp) are filled with large mitochondria. The myoepitheliocytes (me) are rounded off. The cauda (ca) consists of three lobes. bl basal lamina, e esophagus, ecm extracellular matrix, gm glycocalyx-covered microvilli, mca muscle capsule, mf myofibrils, pe pharyngeal epithelium, rER rough endoplasmic reticulum, ve vesicles, vtl ventral tissue lobe, zd z-dots&ig.c:/f
Thus, the maximal number of cuticular rods can be found halfway between the anterior and posterior tips of each row and the number of cuticular rods decreases toward the anterior and posterior tips (Figs. 2–5, 7A: cd, ir, mr, or).
D. Discussion I. Assessment of the features The following discussion is based on the phylogenetic system of the Bilateria as established by Ahlrichs (1995) and Ehlers et al. (1996). Within the Gnathostomulida the discussion partly follows Sterrer′s (1972) recommendation. As all species of the Acanthocephala lack a digestive tract they remain unconsidered here. 1. Pharyngeal musculature The location of the musculature (proximally to the basal lamina) suggests its mesodermal origin (Lammert 1991).
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Fig. 6 Cross-section of the pharynx of G. paradoxa. Non-contractile regions (ncr) separate the muscle capsule (mca) from the caudal muscle pouch (cp) and form the extended ventral tissue lobe (vtl). Basal lamina (bl) surrounds the whole pharyngeal epithelium (pe) and its derivates (nerves and receptors). There is no distinct buccal ganglion separated by a basal lamina. The first gastrocytes (ga) indicate the beginning of the blind intestine. cr contractile regions, ecm extracellular matrix&ig.c:/f
Ax (1956), however, discusses mesodermal as well as ectodermal components for the pharyngeal musculature. Since data derived from ontogenesis are not available (Müller and Ax 1971), the origin of the musculature remains obscure. Isolated z-dots and cross-striated muscu-
lature represent autapomorphies of the Gnathifera (see Ahlrichs 1995) as indicated in the diagram of relationships (Fig. 8: 1). Within the Gnathostomulida, myosyncytia are described only for G. paradoxa and Rastrognathia macrostoma (Kristensen and Nørrevang, 1977, both species of the Bursovaginoidea (see Kristensen and Nørrevang 1977). Species of the Filospermoidea, Rotifera, and Seison lack myosyncytia (Ahlrichs 1995; Koehler and Hayes (1969b). Thus myosyncytia are autapomorphic for the Bursovaginoidea (Fig. 8: 4), whereas the exclusive existence of myocytes in the other taxa represents the plesiomorphic alternative, inherited from the stem species of the Acrosomata (see Ax 1989, 1995).
142 Fig. 7A, B Cross-section of the pharynx of G. paradoxa. A The inner rows (ir) are visible along the inner walls (iw) of the jaw halves. Note that every cuticular rod (cd) consists of an electron-dense core (dc) and an electron-lucent halo (lh). Tonofilaments (tf) run from hemidesmosomes (hs) to desmosomes (not visible here). gc glycocalyx, gm glycocalyx-covered microvilli, mc mouth cavity. B Both rostral wings (rw) of the basal plate form scattered arcs of altogether 14 cuticular rods (cd) at their median margins&ig.c:/f
Extended non-contractile regions are found outside G. paradoxa within species of the Filospermoidea, Rotifera, and Seison (see Ahlrichs 1995). Outside the Grathifera such large non-contractile regions are uncommon. The existence of extended non-contractile regions in the Gnathifera ground pattern might represent an autapomorphy
of this taxon (Fig. 8: 1). A parenchyme or mesenchyme located between the digestive tract and body wall is reported by several authors (e.g. Balsamo 1992). But the present study indicates that species of the Gnathostomulida do not have a distinct parenchyme. Instead, the tissue between the digestive tract and body wall consists
143 Fig. 8 Diagram of the relationships within the Gnathifera (see Ahlrichs 1997). The black squares 1–4 mark autapomorphies&ig.c:/f
mostly of the non-contractile regions of the pharyngeal musculature and of the body wall musculature. Besides G. paradoxa, a muscle capsule and a caudal muscle pouch are described for many other Gnathostomulida (Ax 1956, 1964; Farris 1973; Kristensen and Nørrevang 1977, 1978; Sterrer and Farris 1975). A muscle capsule and a caudal muscle pouch do not exist outside the Gnathostomulida. The muscle capsule and caudal muscle pouch thus constitute autapomorphies in the ground pattern of the Gnathostomulida (Fig. 8: 2). Paired lateral muscle pouches are realized only within a nameless subtaxon of the Bursovaginoidea including Rastrognathia macrostoma, the Onychognathiidae, the Gnathostomulidae, and the Austrognathiidae (Ax 1956; Ehlers and Ehlers 1973; Farris 1973; Kristensen and Nørrevang 1977, 1978; Sterrer and Farris 1975). Paired lateral muscle pouches are absent in Gnathostomaria lutheri (see Ax 1956) and the Filospermoidea, as well as in the other taxa of the Gnathifera. Lateral muscle pouches represent an autapomorphy in the ground pattern of this unnamed taxon. 2. Pharyngeal epithelium Species of the Gnathostomulida (Kristensen and Nørrevang 1977; Lammert 1991; Sterrer 1971), the Plathelminthes (Ahlrichs 1995; Ax 1984; Doe 1981; Ehlers 1985, 1986, 1995, Tyler 1984), and the Euspiralia (Ax 1995) have a pharyngeal epithelium with microvilli covered by a glycocalyx. However, species of the Rotifera (Ahlrichs 1995; Koehler and Hayes 1969b) and Seison (see Ahlrichs 1995) show a pharyngeal cuticle. The existence of a pharyngeal cuticle is an autapomorphy of the Syndermata (Fig. 8: 3). An epithelium without any ciliation is a feature shared by species of the Gnathostomulida (Ahlrichs 1995; Ax 1956; Lammert 1991; Sterrer et al. 1985), Roti-
fera (Ahlrichs 1995; Lorenzen 1996), and Seison (see Ahlrichs 1995). Species of the Plathelminthes (Ax 1984; Doe 1981; Ehlers 1985, 1986, 1995) and Euspiralia (Ax 1995; Purschke and Tzetlin 1996) show the plesiomorphic alternative with a ciliated pharyngeal epithelium. The absence of pharyngeal ciliation is an autapomorphy in the ground pattern of the Gnathifera (Fig. 8: 1). Pharyngeal myoepitheliocytia Paired pharyngeal myoepitheliocytia were also found in Pterognathia meixneri Sterrer 1969 and Haplognathia rosea Sterrer, 1968 (Filospermoidea) (Lammert, unpublished observation). Interestingly, the myoepitheliocytia of these two species show an inverse orientation. Anteriorly, both myoepitheliocytia appear in cross-section not as an erected U, but as a tipped over one. Nevertheless, the myoepitheliocytia of the Filsospermoidea and of G. paradoxa can be homologized. Outside the Gnathostomulida, pharyngeal myoepitheliocytia are unknown for species of the Rotifer, Seison, Plathelminthes, and Euspiralia. Within the Nemathelminthes, pharyngeal myoepitheliocytia are known for the Gastrotricha and the Nematoda. But the pharynges of Gastrotricha and Nematoda species display more than two myoepitheliocytia. A homologization of the myoepitheliocytia of the Gnathostomulida with those of the Gastrotricha and the Nematoda is not possible. Thus paired epithelially embedded pharyngeal myoepitheliocytia can be judged as an autapomorphy of the Gnathostomulida (Fig. 8: 2). 4. Pharyngeal solid parts A pharyngeal jaw in a horizontal resting position and with cuticular rods belongs to the ground pattern of the
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Gnathostomulida (see also Ahlrichs 1995; Ax 1995; Sterrer 1996). The jaw halves and symphysis of the gnathostomulid jaw can be homologized with the manubria and fulcrum of the Rotifera and Seison chewer (see also Ahlrichs 1995, Koehler and Hayes 1969a, b). As hypothesized by Ahlrichs (1995), a jaw or chewer, respectively, represents an autapomorphy of the Gnathifera (Fig. 8: 1). However, a basal plate is an autapomorphy of the Gnathostomulida (see Ax 1995) (Fig. 8: 2).
the lateral muscle pouches and the food is released into the esophagus which has been opened by the contraction of myoepitheliocytes. &p.2:Acknowledgements We are indebted to the collaborators of the II. Zoological Institute for their kind help. This work was supported by the Akademie der Wissenschaften und Literatur, Mainz, and by the Friedrich-Ebert-Stiftung, Bonn.
References 5. Buccal ganglion and buccal nerves A buccal ganglion and paired buccal nerves were described for Rastrognathia macrostoma by Kristensen and Nørrevang (1977). This study shows the absence of a buccal ganglion and of buccal nerves in G. paradoxa (Fig. 6). A reinterpretation of the former study leads to the following conclusion. An accumulation of epithelial nuclei as well as pharyngeal nerves were misinterpreted as a buccal ganglion and buccal nerves, respectively. No basal lamina restricted to this accumulation exists. Thus, the Gnathostomulida lack any buccal ganglion and buccal nerves. 6. Conclusions The assessment of the features discussed in this paper supports the monophyly of the Gnathifera, as well as of the Gnathostomulida, Syndermata, and Bursovaginoidea (Fig. 8). II. Functional aspects The pharyngeal solid parts of G. paradoxa are moved by contraction of the pharyngeal musculature. The force resulting from the muscle contraction is mediated to the solid parts by the force-mediating epithelium characterized by desmosomes, tonofilaments, and hemidesmosomes. The muscle contraction causes a deformation as well as a delocation of the solid parts. After relaxation of the musculature, the solid parts passively return to their original shape by releasing the kinetic energy stored in the cuticular rods. The basal plate moves vertically by contraction of the whole muscle capsule. When sliding forward, the basal plate grasps diatoms, bacteria, or detritus from sediment grains and piles them up. The food is transferred from the mouth opening to the esophagus by the jaw. The jaw halves protrude out of the mouth opening by contraction of the muscle capsule and a simultaneous contraction of the lateral muscle pouches causes the jaw halves to open and surround the food. Relaxation of the lateral muscle pouches closes the rigid jaw halves and then relaxation of the muscle capsule and simultaneous contraction of the caudal muscle pouch move the jaw dorsally, transferring the food to the esophagus. The jaw halves are opened again by contraction of
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