Acanthocephala)

Proc. Helminthol. Soc. Wash. 51(2), 1984, pp. 221-224

A Support Cell to the Apical and Lateral Sensory Organs in Moniliformis moniliformis (Acanthocephala)

DONALD M. MILLER AND T. T. DUNAGAN Department of Physiology, Southern Illinois University, Carbondale, Illinois 62901

ABSTRACT: A large cell containing five nuclei is described adjacent to the proboscis sheath and ventral to the middle or anterior part of the cerebral ganglion in Moniliformis moniliformis. Four tubelike ducts or processes exit the body of this cell identified as the sensory support cell. The two posterior extensions penetrate the proboscis sheath and join the ventral proboscis retractor muscles. These processes gradually move together as they extend anteriorly and fuse into a single process slightly anterior to the cerebral ganglion. This single duct continues anteriorly surrounded by proboscis retractor muscles and eventually terminates in the apical organ. Each of the two anterior processes joins the ventral anterior medial nerve. Parts of the nerve and each duct move laterally as they extend anteriorly and terminate in the lateral sensory organ.

The discovery (Miller and Dunagan, 1983) of of surfaces conformed to earlier usage by German au- a multinucleated cell ventral to the cerebral gan- thors (Hamann, 1891; Kaiser, 1893; Rauther, 1930; glion in Macracanthorhynchus hirudinaceus sug- etc.). gested that a similar cell might occur in other Results species. That this was not an isolated event was The position, size, and shape of the sensory also suggested by Harada's (1931) original report support cell varied somewhat from specimen to of a "stutzzelle" near the cerebral ganglion of specimen presumably depending on the size of Bolbosoma turbinella. In each of these species, the worm and the technique used to prepare the this support cell had extensions that terminated material for study. Isosmotic washes and fixation in the lateral sensory organs in B. turbinella and maintained the SSC pressed between the recep- both lateral and apical sensory organs in M. hi- tacle protrusors and the proboscis sheath that rudinaceus. The former is a member of the Pa- flattened the cell and caused less taper along its laeacanthocephala, and the latter belongs to the longitudinal axis. The SSC was located adjacent Archiacanthocephala. to the proboscis sheath and along its ventral sur- This paper describes a sensory support cell in face in the vicinity of the middle to upper third Moniliformis moniliformis (=M. dubius) and of the cerebral ganglion (Figs. 1, 2). A typical compares this cell with the two similar cells that measurement at maximum dimensions was 80 have previously been described. /um long x 55 yum wide x 14 /urn thick. The lat- Materials and Methods eral view (Fig. 1) of the SSC indicates that the thickness varied throughout but primarily at the Moniliformis moniliformis was raised in Sprague anterior and posterior extremities. Dawley rats from intermediate stages provided by Dr. Jane Starling of University of Missouri at St. Louis. The SSC cell body contains five nuclei of ap- Adult worms were fixed, embedded, stained, and sec- proximately the same size. Three of these nuclei tioned according to routine techniques (Dunagan and are visible in Figure 6. The level of this section Miller, 1976). However, prior to fixation, the worms is indicated on Figure 2. Note that each nucleus were placed overnight into distilled water in a refrig- erator. This hyposmotic solution causes the body and has a prominent round nucleolus. praesoma to swell. This influx of water tended to sep- Arising from the SSC soma are four tubelike arate internal structures, which in this case were the extensions (Fig. 2). The two posterior lateral pro- receptacle protrusor muscles, from the cerebral gan- cesses penetrate the proboscis sheath and asso- glion. Although this disrupted the normal relationships ciate with the origin of the ventral part of the between components, it also enabled one to clearly view the sensory support cell (SSC) that otherwise was proboscis retractor muscles (Fig. 7). The ducts so tightly packed between the receptacle protrusors, move to the medial surface of these muscles, and proboscis sheath, and cerebral ganglion, that it was as they extend in an anterior direction, they grad- difficult to differentiate from other surrounding struc- ually move together until they fuse into a single tures. The ventral surface was determined according to Hy- tube (Fig. 3). This sequence of events is shown man (1951, p. 5) who used the position of the cerebral in Figures 3-5 whose representative level of sec- ganglion as the determining factor. Her identification tioning has been indicated on Figure 2. Figure 4 221

the cerebral ganglion of M. moniliformis. He il- lustrated a structure ventral to the ganglion la- beled "Markraum" that showed two nuclei. This is the same structure that we now identify as the SSC. Likewise, we published photographs of the cerebral ganglion of M. moniliformis in which the SSC may be seen as a cap on the convex surface of the CG (Dunagan and Miller, 1975, fig. 5-C; 1976, fig. 5). Previous descriptions of this type of cell were made by Harada (1931) and Miller and Dunagan (1983). Harada described this cell in Bolbosoma turbinella as anterior to the ganglion in the space between the dorsal proboscis retractors and the proboscis sheath. We described the cell in M. hirudinaceus as ventral to the ganglion on the external surface of the midventral longitudinal receptacle muscle. We do not believe that the sensory support cell (Stiitzzelle) is dorsal in one species and ventral in another but that this is a problem of misinterpreting surfaces. Our direc- tions are based on Hyman's (1951) statement that the cerebral ganglion in Acanthocephala is nearest the ventral surface. Her illustration (fig. 9) of a cross section of the proboscis through the LATERAL cerebral ganglion (after Luehe, 1912) clearly la- Figures 1-2. Diagrammatic representations of the beled the structures on this surface as ventral. sensory support cell from Moniliformis moniliformis. On that basis, the sensory support cell in M. Abbreviations: N, nucleus. 1. Lateral view. 2. Ventral view. hirudinaceus and M. moniliformis is ventral to the ganglion. Harada (1931, p. 171) stated that the ganglion in B. turbinella was almost in the center of the proboscis sheath. However, his de- shows the posterior ducts adjacent to each other scription of the ganglion clearly shows that his but prior to fusion. After fusion, this single duct designation of dorsal surface corresponds to our continues anteriorly enclosed by the proboscis designation of ventral surface. Thus, the support retractor muscles until it penetrates the apical cell is located on the same side of the cerebral sense organ. It is accompanied by the apical sen- ganglion in each of the three species so far de- sory nerves (medial pair) and the anterior pro- scribed. boscis nerves (outer pair). The latter do not pen- Harada described the support cell as "U"- etrate the apical organ but service muscles in the shaped and consisting of two cells joined at their apical region. base with anterior extensions that serviced the The anterior extensions of the SSC (Fig. 7) join lateral sensory organs. However, he indicated (p. a large group of nerves from the anterior part of 175) that nerve fibers did not penetrate these the cerebral ganglion. Each of these anterior ducts organs and that the extensions of the support cell along with several nerves extend anteriorly, grad- did not always terminate in a papilla but rather ually moving laterally in the process. Each of the were sometimes flattened without penetrating the anterior extensions terminates in a lateral sen- surrounding muscle layers. Neither of these ob- sory organ. servations are consistent with the morphology of the support cell in M. hirudinaceus or M. mo- Discussion niliformis. The latter have a single multinucleat- The sensory support cell of M. moniliformis ed cell that services the apical and lateral sense has previously appeared in published drawings organ and that is also serviced by neurons. or photographs. Kaiser (1893) published a dia- In 1943, von Haffner (p. 81) indicated that a gram (plate VIII, fig. 34) of a cross section through median nerve extended from the cerebral gan-

Figures 3-7. Cross sections of sensory support cell and its extensions. Abbreviations: AD, anterior duct from lateral anterior margins of support cell. CG, cerebral ganglion. PD, posterior duct from posterior half of support cell. PR, proboscis retractor muscle. RP, receptacle protrusor muscle; RW, receptacle wall muscle. SSC, sensory support cell. Position of certain sections indicated on Figure 2. 3-5. The fusion of the PD into single process. 6. The position of the SSC. 7. The relative positions of AD and PD following the separation of the AD from the soma of the SSC. Scale in Figure 3 applies to Figures 4, 5. Scale in Figure 6 applies to Figure 7. glion to the anterior end of O. thumbi where it was actually the fused posterior extensions of the formed a "Endaufknauelung." He later (p. 82) sensory support cell. Indeed, von Haffner (1943, stated that the median nerve divided into two p. 89) compared his description of the median branches upon entry into the "Muskelplatte," nerve in O. thumbi with the median nerve in M. which from his drawing we would interpret as hirudinaceus indicating that their organization the posterior part of the apical organ. This same and location were of the same type. This rein- nerve was described by von Haffner (1943, p. 86) forces our belief that a reexamination of O. as originating from two separate nerves in the thumbi would show that the previously described "vorderen Fla'che des Ganglion." These two branches of the median nerve do not enter the nerves then united to form the single median cerebral ganglion, but are extensions of a cell nerve. We believe that von Haffner may have ventral to but in close proximity to the cerebral made the same mistake in identifying the median ganglion. If this is true, then von Haffner's con- nerve that we and others (Kaiser, 1893; Kilian, clusion that the median nerve branched upon 1932; etc.) have made. His description matches entering the apical sense organ and formed the our earlier discovery (Miller and Dunagan, 1983) "Endaufknauelung" or terminal ball of coiled that the anterior medial nerve in M. hirudinaceus nerves will also need to be reconsidered. Fur-

Copyright © 2011, The Helminthological Society of Washington 224 thermore, his description of the four motor nerves togenie, Anatomic, nebst Beitragen zur Systematik that accompany the median nerve may also need und Biologic. Jenaische Zeitsch. Naturwiss. 25: 113-231. revision. He described them as passing over the Harada, I. 1931. Das Nervensystem von Bolbosoma external surface of the apical organ to service the turbinella (Dies.). Jap. J. Zool. 3:161-199. muscles associated with the proboscis hooks. If Hyman, L. H. 1951. The Invertebrates. Vol. III. they follow the M. hirudinaceus model as he sug- Acanthocephala, Aschelminthes, and Entoprocta. McGraw-Hill, New York. gested, the medial pair of these nerves enters the Kaiser, J. E. 1893. Die Acanthocephalen und ihre apical organ and the lateral pair divides near the Entwickelung. 2 Theil (R. Leuckart and C. Chun, posterior terminus of the apical organ and ex- eds.). Cassell. Biblioth. Zool. 7:1-148. tends over its external surface before further di- Kilian, R. 1932. Zur Morphologic und Systematik visions occur. der Giganthorhynchidae (Acanthocephala). Z. Wiss. Zool. 141:246-345. Miller, D. M., and T. T. Dunagan. 1983. A support Literature Cited cell to the apical and lateral sense organs in Macra- Dunagan, T. T., and D. M. Miller. 1975. Anatomy canthorhynchus hirudinaceus (Acanthocephala). J. of the cerebral ganglion of the male acanthoceph- Parasitol. (In press.) alan, Moniliformis dubius. J. Comp. Neur. 164: Rauther, M. 1930. Sechste Klasse des Cladus Ne- 483-494. mathelminths Acanthocephala-Kratzwurmer. , and . 1976. Nerves originating from (Kiikenthal and T. Krumbach, eds.) Handbuch der the cerebral ganglion of Moniliformis monilifor- Zoologie. 2 Band, 1 Halfte, pp. 449-482. mis (Acanthocephala). J. Parasitol. 62:442-450. von Haffner, K. 1943. Die Sinnesorgan an der Rus- Hamann, O. 1891. Monographic der Acanthoce- selspitze von Acanthocephalen. Z. Morph. Oekol. phalen (Echinorhynchen). Ihre Entwickelung, His- Tiere. 40:80-92.