AN ULTRASTRUCTURAL APPROACH TO FEEDING BEHAVIOUR IN PHILODINA ROSEOLA AND BRACHIONUS CALYCIFLORUS (ROTIFERS)

II. THE OESOPHAGUS

P. CLgMENT, J. AMSELLEM, A.-M. CORNILLAC, A. LUCIANI’ & C. RICCI’

’ Laboratoire d’Histologie et Biologie Tissulaire (LA 24 CNRS) et CMEABG, Universitt Claude Bernard (Lyon I), Villeurbanne, France; ’ Instituto di Zoologia, Universita degli studi, via Celosia, IO, Milano, Italy

Keywords: Rotifer, ultrastructures, feeding behaviour, digestive tract, cuticle

Abstract

The cuticular oesophagus is a simple expansion of the dorsal pharyngeal wall of the mastax. The ciliary oesophagus is the cel- lular anterior wall of the stomach lumen, but seems to have the same embryological origin as the pharynx.

In Brachionus calyciflorus, its cilia are surrounded by cuticular velums which have the same myelin-like structure and the same function as the buccal velum of Philodina roseola. In all cases, the oesophagus prevents the return of food particles from the stomach to the mastax lumen.

Introduction

Criteria to distinguish the end of buccal structures from the beginning of pharyngeal structures are: the character- istic buccal and pharyngeal cilia and the buccal velum, which originate from apical membranes of the anterior pharyngeal cells.

In this paper, we describe the end of the pharynx. Clas- sical studies note the existence of an oesophagus between the mastax and the stomach (De Beauchamp, 1909,1965; Remane, 1929-1932; Hyman, 1951). Its ultrastructure was briefly described in Trichocerca rattus by Cltment (1977a,

b) but Schramm (1978) did not find an oesophagus in Habrotrocha rosa. Thereby she incorrectly called a part of the buccal tube an oesophagus.

After meticulous observations which we think are not as widely known as they should be, De Beauchamp (1909) distinguished the cuticular oesophagus from the ciliary oesophagus. The former has the same cuticle as the pharynx. The latter is the upper part of the stomach be- tween the cuticular oesophagus and the gastric glands. Each of these two sectors can be either short or long, de- pending on species. Unfortunately, classical drawings of Rotifers (Remane, 1929-1932; Hyman, 1951; Ruttner- Kolisko, 1974; Koste, 1978) show a uniform oesophagus,

and ignore the distinction made by De Beauchamp ( I 909). Our ultrastructure observations show that the cuticular

oesophagus is a pharyngeal expansion, and confirm the existence of a ciliary oesophagus whose features are very different from the stoma&s.

Results (Material and methods: see Cltment et al., I98oa)

Philodina roseola: (Fig. I to 4) The cells of the dorsal mastax roof extend backwards to constitute the thin epithelial wall of the cuticular oeso- phagus (Fig. 2). This oesophagus does not have its own epithelial cells. Its fine epithelial wall is doubled by a muff of muscle cells (Fig. 3). These muscle cells have only a few myofilaments, which are grouped together near the epithelial tube.

In P. roseola, the stomach is syncitial and its lumen is bordered by a special terminal web, described by Mattern h Daniel (1965), and by Schramm (1978) in H. rosa. Be- tween the stomach and the cuticular oesophagus, there exists a short ciliary oesophagus, made of ciliated cells (Fig. I and 2). These cilia are very long. They form the vibratile flame beating in the stomach lumen (Fig. 2).

The big gastric glands of P. roseola arrive in the ciliary oesophagus (Fig. 3 and 4).

Brachionus calycQi’orus: (Fig. 5 to 8) The cuticular oesophagus is shorter. It is also a simple pharyngeal epithelium expansion (Fig. 6). The cuticle is thicker than in P. roseola: it is made of a membrane-pile (Fig. 5 and 8). This membrane-pile separates from the pharyngeal epithelial cells, to form a cuticular velum which has the same structure as the buccal velum; it also has a fish-trap form (Fig. 6). Just under this ‘cuticular velum’, there are cilia borne by the cells of the very short ciliary oesophagus (Fig. 5 and 6). Meanwhile, the epi-

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Hydrobiologia 73, 133-136(1980). 0018-8158/80/0732-0133$‘00.80. 0 Dr. W. Junk b.v. Publishers, The Hague. Printed in the Netherlands.

Figs. 1-4. Philodina roseola. Fig. I. x IOWO. Cuticular oesophagus (QO) and ciliary oesophagus (CO): the cilia (C) are borne by ciliary cells (CC). The gastric gland (G) opens at the level of these cells. (ST) stomach syncitium; Fig. 2. x 3000. The lumen ofthe stomach syncitium (ST) contains the ciIia which come from the cihary oesophagus (CO). The cuticular oesophagus (QO) is in continuity with the dorsal pharyngeal epithelium of the mastax, which bears the striated pharyngeal cilia (MA). Syn- cytial gastric gland (G); Fig. 3. x 16400. A muscle cell (Mu), with its nucleus (N) is located around the epithelial wall (E) of the cuticular oesophagns. This cell (E) bears only a few cilia (arrow) when it is in contact with the upper part of the stomach lumen (L). See also Fig. I. Most cilia are borne by epithelial cells (C) of the ciliary oesophagus. (G) = gastric gland; Fig. 4. x 6000. The arrow shows the communication between the mastax lumen (at left) and the cuticular oesophagus lumen: the epithehal cytoplasm and the cuticle are strictly the same. At right, a part of ciliary oesophagus

and gastric glands (G).

Figs. 5-g. Brachionus calyciflorus. Fig. 5. x 20000. Detail of an axial section of the cuticular (QO) and ciliary (CO) oesophagus. At this level, the cilia(C) are located between the median velum (V) and the ftne cuticle (arrow) of the ciliary c&l; Fig. 6. x 6500. Axial section of the cuticular oesophagus (QO) and ciliary oesophagus (CO). The cuticle which lines the mastax lumen (L) extends in the cuticular oesophagus, and then forms a velum (V). Lining this velum are the cilia of the ciliary oesophagus; these cilia are separated from the stomach lumen (SL) by a new cuticilar velum (arrow) which comes from the ciliary oesophagus I35 (CO). (S) = stomach cell. M = a muscular cell; Fig. 7. x 9500. Opening of the two velums in the stomach lumen (SL). The principal median velum (V) lines the end of the oesophagus lumen. The secondary cuticular velum (arrows) sepa- rates the oesophagus cilia from the stomach lumen, except at the extremity of the cilia(C); Fig. 8. x I 27000. High power

magnification of the cuticle of the cuticular oesophagus which shows a myelin-like aspect.

thelial cells of this ciliary oesophagus show also an apical cuticle (Fig. 5 and 6). This cuticle gives a second cuticular velum which surrounds the first. All this forms a vibratile flame with the cilia located between the two velums (Fig. 6). The internal velum opens into the stomachal lumen at the vibratile-flame extremity (Fig. 7): the food particles pounded by the mastax, go by this way. The cilia also end in the stomach lumen at the vibratile-flame extremity (Fig. 7).

The two parts of the oesophagus form a short epithelial structure not surrounded by a muscular layer: there is only a circular ring where the mastax lumen narrows to form the cuticular oesophagus lumen (Fig. 6).

Conclusions

Functions of the oesophagus: In the two observed species, the food particles once in the stomach cannot go back into the pharynx. The cuticular oesophagus divides the digestive tube into compartments: it has the same function as the buccal velum in the more anterior region. Two different systems are used for this: muscles in P. roseola, and cuticular velums with a fish- trap form in B. calyczflorus.

On the other hand, the vibratile flame borne by the

Fig. 9. Diagram of the digestive tract of a Rotifer.

ciliary oesophagus, allows the food to progress into the stomachal lumen.

Nature of the oesophagus: (Fig. 9) The cuticular oesophagus is only a pharyngeal expansion. The ciliary oesophagus is made of epithelial cells. These distinct cells do not look like the cells or the syncitium which form the stomach wall: in particular stomachal cilia are shorter and have no ciliary rootlets.

On the other hand, in B. calyciflorus, these epithelial cells look like the pharyngeal epithelial cells: they have the same multimembranous cuticle and they can form a cuticular velum. So it is possible that the ciliary oeso- phagus has the same embryological origin as the pharynx (stomodeal imagination), while the stomach seems to come from the dorsal ectoderm (Nachtwey, 1925; De Beauchamp, I 965).

References

De Beauchamp, P. 1909. Recherches sur les Rotiferes: les forma- tions tegnmentaires et l’appareil digestif. Arch. Zool. exp. gen., 10: 1-410.

De Beauchamp, P. 1965. Classe des Rotiferes. In: ‘Trait& de zoologie, anatomie, systematique, biologie. P. Gras&, IV, 3: 1225-1379.

Clkment, P. i977a. Introduction a la photobiologie des rotiferes dont le cycle reproducteur est contrBle par la photoptriode. Approches ultrastructurale et experimentale. These no 7716, Universitt Claude Bernard (Lyon I): 262 pp.

Clement, P. r977b. Ultrastructural research on Rotifers. Arch. Hydrobiol. Beih., 8: 270-293.

ClCment, P., Amsellem, J., Cornillac, AM., Luciani, A. & Ricci, C. t98oa. An ultrastructural approach to the feeding behaviour of Philodina roseola and Brachionus calyciflorus. I. The buccal velum. In this VOhme, pp. 127-131.

Hyman, L. H. 1951. Class Rotifers. In: ‘The invertebrates’, MC Graw Hill, New York, vol. 3, pp. 59-151.

Koste, W. 1978. Rotatoria. Borntraeger, Berlin, 2 vols., 673 pp., 234&ZlteS.

Mattern, C. F. T. & Daniel, W. A. 1965. The stomach cell of Rotifer. Electron microscope observations of the terminal. Web. J. Cell. Biol., 29: 547-551.

Nachtwey, R. I 925. Untersuchungen fiber die Keimbahn Organo- genese und Anatomie von Asplanchna priodonta Gosse. Z. Wiss. Zool., 126: 239~492.

Remane, A. 1929-1932. Rotatoria. In: ‘Dr. HG. Bronn’s Klassen und Ordnungen des Tier-Reichs’, IV (Vermes), 2 (Aschel- minthes), I (Rotatorien, Gastrotrichen und Kinorhynchen), 3: 1-448.

Ruttner-Kolisko, A. 1972. Rotatoria. Binnengewtisser, 26: 99- 234.

Schramm, U. 1978. Studies on the ultrastructure of the Rotifer Habrotrocha rosa Donner (Aschelminthes). The alimentary system. Cell. Tiss. Res., 189: 525-535.

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