Species Diversity, 1998, 3, 17-24

Cysticolous Myzostomida, Notopharyngoides platypus from Comanthina nobilis (Echinodermata: Crinoidea), at Kushimoto, Honshu, Japan

Mark J. Grygier1 * and Keiichi Nomura2**

'Tropical Biosphere Research Center (Sesoko Station), University of the Ryukyus, Sesoko 3422, Motobu, Okinawa 905-0227, Japan 2Kushimoto Marine Park Center, Arita 1157, Kushimoto, Wakayama 649-3514, Japan

(Received 17 February 1997; Accepted 3 September 1997)

About 20% of individuals of the comatulid crinoid Comanthina nobilis (Carpenter, 1884) at Shionomisaki, the southernmost point of the island of Honshu, Japan, are infested by the cysticolous myzostomidan worm originally described asMyzostoma platypus Graff, 1887. Up to four cysts per host occur. This parasite had been collected previously only in the Philippines by the 'Challenger' Expedition, from the same host species. The present specimens differ in having a few to many supernumerary marginal cirri and up to six (versus three to five) separate tabular outgrowths in a row along the ventral midline. It is proposed to reassign this species as the most plesiomorphic member of the genus Notopharyngoides Uchida, 1992. Key Words: Myzostomida, Notopharyngoides platypus, Crinoidea, Comanthina nobilis, Japan, redescription, range extension, cysticole, marine parasitology.

Introduction

Carpenter (1888) described in detail the comasterid crinoid Actinometra (now Comanthina) nobilis Carpenter, 1884 based on the holotype from 'Challenger' sta. 208 (Philippines, 11°37'N, 123°31'E, 33m) and five additional specimens from Samboangan (i.e., Zamboanga, Philippines); he had formerly considered the latter as representing a distinct species. The holotype of A. nobilis and one of the other specimens bore uncalcified cysts on the disc, and the aperture of each cyst opened close to an ambulacral groove. Carpenter (1888: pi. LXV, fig. 8) illustrated three such cysts on one host, a specimen from Zamboanga according to Carpenter's letter quoted by Graff (1887). Perhaps in error, this letter said there were six specimens of A. nobilis from that place, not only five. Carpenter sent another cyst from the same host individual to Graff, who described the single myzostome found therein as Myzostoma platypus (see Graff 1887:13-14, pi. Ill, figs 7-12). Graffs holotype of M. platypus was not found (by MJG) among other 'Challenger' material during a visit to The Natural History Museum in London in 1986. The only subsequent study of M. platypus was a histological investigation by Wheeler (1896:244-246, 276, 279-280, pi. 11, figs 26-30). lie found a specimen of A. nobilis in the London museum with many cysts on the disc and arm bases, removed the single myzostome from nine of them, and sectioned eight worms; these sections

*Current address: Lake Biwa Museum, Oroshimo 1091, Kusatsu, Shiga 525-0001, Japan " Current address: Yaeyama Marine Park Research Station, Kuroshima, Taketomi, Okinawa 907-1311, Japan 18 M. J. Grygier and K. Nomura are currently housed in The Natural History Museum, but the unsectioned specimen was not found there in 1986. Wheeler neglected to mention where the crinoid had been collected. All the sectioned specimens were late hermaphrodites with reduced male organs. Wheeler (1896) also found from one to five endoparasitic trematodes, which he named Disloma myzostomatis, in the parenchyma of the wall of the pharynx (i.e., the introvert) in each sectioned specimen. In a review of crinoid associates, Clark (1921) reported the host of M. platypus as Comanthina schlegelii (Carpenter, 1879), but Rowe et al. (1986) once again recog nized C. nobilis as a separate species. Clark (1921) reported Singapore as well as Zamboanga as a locality for this myzostome, but we have been unable to find a record from Singapore in any primary literature and assume that Clark was mis taken.

Family Myzostomatidae Beard, 1884 Genus Notopharyngoides Uchida, 1992 Notopharyngoides platypus (Graff, 1887), n. comb.

Material. Prevalence (frequency of infestation) of Comanthina nobilis at Shionomisaki, Kushimoto, Honshu, Japan, about 20%, with one to four cysts per infested crinoid (Fig. 1). Specimens examined in detail include three from one host, 6 November 1996, coll. K. Nomura (crinoid caught in lobster net) and two specimens from another host, 7 December 1996, 15 m, coll. K. Nomura (SCUBA). Host species identified (by KN) using key of Kogo (1995). All specimens deposited in Osaka Museum of Natural History (OMNH-Iv 1495-1499). Disc of second infested crinoid, a dissected cyst from first crinoid, and worms isolated from both hosts were photo graphed; worms were also examined under binocular dissecting microscope. Two 'parapodia' (right legs 3 and 4) of damaged specimen partly dissolved in weak bleach and mounted on slide in glycerine jelly in order to study hook apparatus under compound microscope. Description of cyst. Only one intact cyst examined in detail (Fig. 2a): irregularly subspherical, about 4.8mm long and 4.0mm wide, soft and uncalcified, with 1.3mm diameter circular aperture adjacent to ambulacral groove, and lip of latter notched at that spot. Myzostome within cyst (Fig. 2b,c) oriented with posterior end toward aperture and ventral side upwards. Description of myzostome. Specimens round to oval and highly convex ventrally, variably concave dorsally (Figs 2-4). Dorsal side smooth. One specimen from first host (not illustrated) 4.15mm in diameter, its dorsum 3.8X 3.3mm, askew from normal body axes; another specimen damaged (nearly cut in half transversely), 5.65mm wide; third specimen (Fig. 2b,c) 4.1mm wide, 3.9mm long. One specimen from second host (Fig. 4) with dorsum 4.1mm long, 3.5mm wide, the other specimen (Fig. 3) 2.8mm long, 3.6mm wide. Body margin developed into membranous, cirrus-bearing flange in one specimen, but not especially thin in other specimens. Two specimens with 21 marginal cirri each, and another with 23, arranged somewhat irregularly (missing from a few sites if meant to be spaced evenly, and including small posterior clump of supernumerary cirri, some of these bifid). Another specimen with 30 marginal cirri [one cirrus bifid (Fig. 3b) and supernumerary ones mostly at rear], and the last with 45-46 cirri Cysticolous Myzostomida Notopharyngoides platypus 19 spaced quite unevenly and including two bifid cirri and one multifid cirrus. On ventral side, no submarginal shelf or lappets present, but fairly distinct line in one specimen marks boundary of some sort near edge. Row of six flat-topped, sometimes apically flared outgrowths along ventral midline in two specimens (Fig. 2b), first such process longest, remainder more or less round to cat's-eye-shaped. In another individual, second and third processes narrowly joined. In two others (Figs 3a, 4), both second and third, and fourth and fifth joined. In all specimens, introvert pouch opening at base of front end of first mid-ventral process (Fig. 5). Ano-genital opening, when visible, found at posterior edge of rearmost process or, in one specimen, on barely separated ano-genital cone behind it, in each case quite close to body margin. Introvert fully retracted (Fig. 2c) or with its distal end exposed (Fig. 4b) or fully protruded (Fig. 3). Total length of introvert up to 1.5 mm. Conical, radially furrowed distal part of introvert enclosing laterally compressed mouth and surrounded by lip bearing corona of seven or eight pairs of triangular, distally acuminate buccal papillae (number varying among three specimens in which they could be counted accurately). Gap between ventralmost pair of papillae. Five pairs of 'parapodia' (legs; best displayed in Fig. 4a), each with stubby, blunt distal part arising from gap in broad, heart-shaped proximal fold. In one specimen, outer lobes of these folds sometimes bent away from general body surface. Folds of similar size in all legs, except sometimes one or both of fifth pair smaller. Hook apparatus consisting of hook, smaller replacment hook of variable size, and support rod (Fig. 6). Hooks in examined specimen 656-670/zm long, 56//m wide, distal quarter bowed very slightly outward and tip forming an evenly tapered, rounded hook of less than 90°. Support rods 25% longer than hooks, slightly thicker than hooks for most of length but almost 40% thicker at base, distal third tapered and slightly curved; interior of shaft hollow distally; manubrium developed only on inner side of tip, curving around inner margin of hook and bearing many small, rounded, irregularly placed lobules along its own inner margin. Third pair of 'parapodia' associated with pair of penes up to 2.1mm long arising from their outer bases. Two specimens with one penis protruded like large, tapered, translucent cannon (tip may be curved) and other penis retracted as small knob (Fig. 3). In another specimen, one penis fully protruded, the other one halfway so (Fig. 5). In damaged specimen, right penis lost, but left one long and thick with abnormally swollen distal part and narrow tip (Fig. 5). In final specimen, both penes protruding equally but not reaching body margin (Fig. 2b). Four pairs of large, circular, distinctly yellowish lateral organs (in contrast to creamy white color of remainder of formalin-preserved body), each centered about halfway between outer edges of 'parapodia' and body margin, similar in form but protruding to different degrees in different specimens (best displayed in Fig. 3a). Lateral organs consisting of short stalk, outer ring with diameter greater than stalk, more heavily pigmented but narrow ring inside this, and inner dome-like zone with exposable and protrusable central button; when button exposed, inner rim of dome radially grooved. Remarks. The present specimens differ from those described by Graff (1887) and Wheeler (1896) in having more than 20 marginal cirri (in two cases many more) and in having up to six rather than three to five mid-ventral processes. However, in Graff's (1887) drawing the fourth mid-ventral process corresponds to the coalesced 20 M. J. Grygier and K. Nomura

Figs 1-5. Notopharyngoidesplatypus (von Graff, 1887) from Kushimoto, Japan; microphotographs with scale bars in mm. Fig. 1. Two cysts (arrows) on disc of living Comanthina nobilis, host of OMNH-Iv 1495-1496. Fig. 2. Preserved cyst and contents (OMNH-Iv 1499): a, cyst dissected Cysticolous Myzostomida Notopharyngoides platypus 21 processes 4 and 5 of the present specimens; in the specimen drawn by Wheeler (1896), the same is true and the equivalents of processes 2 and 3 are also coalesced. Probably six is the fundamental number of these processes, but the second and third, and fourth and fifth, may commonly be confluent. Graff (1887) illustrated the inner margin of the parapodial support rod's manubrium as evenly serrate, while in the present examined specimen it bears irregularly placed small lobules. The holotype was oriented with its anterior end toward the cyst aperture (Graff 1887), unlike the specimen described here. Either the bowed body shape permits the introvert to reach outside the aperture regardless of orientation, or the worm is capable of movement within the cyst. The preponderance of posterior supernumerary cirri, which may have arisen following injury, also suggests that the posterior end is typically kept in the most exposed position, near the cyst's aperture. In his description of Myzostoma aruense, Remscheid (1918) remarked on its resemblance toM platypus, and Jagersten (1937) furthermore argued thatM ijimai Hara & Okada, 1921 stood close to both. [Hara and Okada (1921) did not explicitly compare their new species to any other.] Jagersten (1937) considered that certainly M. ijimai and M. aruense, and not improbably M. platypus as well, would belong together if Myzostoma were split up into different genera. Fishelson (1974, 1976) treated M. ijimai, misspelled as ijimani, as belonging to an undefined (and thus unavailable at that time) genus, Notopharyngoides. This name was apparently coined by Fishelson's Russian consultant, V. L. Wagin, who never published it except as a nomen nudum in a biogeographical context, so far as we have been able to determine. However, Uchida (1992) inadvertently diagnosed Notophayngoides by the dorsal mouth opening and thus validated this genus, with the type species N. ijimai (see historical account by Grygier 1994). Eeckhaut et al. (in press) accepted the validity of this genus, which is readily defined by unambiguous apomorphies. All three species have in common a row of flat-topped outgrowths along the ventral midline with the ano-genital pore at the rear of the most posterior one, as well as large, heart- or kidney-shaped plates developed from the proximal folds of the 'parapodia'. However, N. ijimai and N. aruensis have a common set of additional peculiarities [see Eeckhaut et al. (in press) for a redescription of N. aruensis]: a dorsal opening of the introvert pouch and thus the separation of this opening from the anterior midventral process, absence of buccal papillae, absence of marginal cirri, a continuous or interrupted ventral submarginal fold (if discontinous, as a series of lappets) and commonly the coalescence of certain lateral organs with this fold (or lappets), usually only three midventral outgrowths possibly representing fusions of those in N. platypus, each free lateral organ as the protrusible central part of a large, flat, circular plate (in N. platypus the lateral organs are greatly enlarged, but their outer regions are not reduced to an inert plate), the ano-genital pore located just at the base

from host crinoid, showing ambulacral groove of latter (arrow); b, c, myzostome removed from cyst in ventral and dorsal views, respectively, with anterior end at top. Fig. 3. Specimen with protruding introvert (i) and penis (p) (OMNH-Iv 1496): a, in life, ventral view; b, preserved, dorsal view, with dorsal surface over base of introvert damaged and arrow pointing to bifid marginal cirrus and supernumerary cirrus. Fig. 4. OMNH-Iv 1495: a, in life, ventral view with protruding penis, anterior end right; b, preserved, anterior view with fully and partly protruded penes (p) and retracted introvert (i). Fig. 5. Aberrant swollen penis of preserved OMNH-Iv 1498. Fig. 6. Notopharyngoides platypus (von Graff, 1887) (OMNH-Iv 1498), 'parapodial' hook apparatus, including hook (h), replacement hook (r), and support rod (s): A, of right leg 3; B, of right leg 4. Scale bar in mm. Cysticolous Myzostomida Notopharyngoides platypus 23

(rather than at the rear apex) of the last midventral process, and fully separate 'nephridia' [i.e., utero-intestinal ducts; they have a common 'nephrostome' in N. platypus (Wheeler 1896)]. In addition, Af. aruensis has a much more robust parapodial hook apparatus than the present species (cf. Eeckhaut et al. in press). All three species are probably ordinarily endosymbionts. Notopharyngoides ijimai has usually been found inhabiting cysts singly or in pairs on its host's disc, although Jagersten's (1937) specimens were from the esophagus, while N aruensis (or forms closely related to it) has often been found in the host's gullet (Eeckhaut et al. in press). Remscheid's (1918) specimens of N. aruensis were supposedly free-living, which Jagersten (1937) found unbelievable. Of the great number of apomorphies relative to ordinary species of Myzostoma that are shared by N. ijimai and N. aruensis (and possibly other species currently assigned to the latter: Eeckhaut et al. in press), N. platypus has two fully developed (the midventral processes and the 'parapodial* lobes) and one in a transitional state (the enlarged lateral organs). These features serve to diagnose the genus Notopharyngoides. By most morphological features, N. platypus is the most plesiomorphic species currently assigned to this genus. The exception concerns the partly fused and thus apomorphic utero-intestinal ducts ('nephridia') of N. platypus. The known geographic range of N. platypus is the Philippines and Japan. However, the range of its host, Comanthina nobilis, also includes a swath of the tropical Indo-West Pacific from Sri Lanka, through Singapore, Indonesia, and the northern half of Australia, to New Caledonia (Rowe et al. 1986), and we assume that N. platypus can be found over most or all of that range.

Acknowledgements

Dr. T. Oji (Geological Institute, University of Tokyo) and Ms. C. Ahearn (National Museum of Natural History, Smithsonian Institution) provided informa tion from crinoid literature. This work was done during MJG's appointment as a C.O.E. Visiting Foreign Researcher at the Tropical Biosphere Research Center (Sesoko Station), University of the Ryukyus.

References

Beard, J. 1884. On the life-history and development of the genus Myzostoma (F. S. Leuckart). Mitthcilungen aus dem Zoologischen Station zu Neapel 5: 544-580, Pis. 31-32. Carpenter, P.H.C. 1888. Report on the Crinoidea collected during the Voyage of H.M.S. Challenger during the years 1873-76. Part II. The Comatulae. Scientific Results of the Voyage of H.M.S. Challenger during the Years 1873-76. Zoology 26(60): ix + 1-339, Pis. I-LXX. Clark, A.M. 1921. A monograph of the existing crinoids. Vol. 1. The comatulids. Part 2. Bulletin of the United States National Museum 82(2): xxv+1-795, Pis. 1-57. Eeckhaut, I., Grygier, M.J. and Deheyn, D. In press. Myzostomida from Papua New Guinea with related Indo-West Pacific records and descriptions of five new species. Bulletin of Marine Science 63(2). Fishelson, L. 1974. Ecology of northern Red Sea crinoids and their epi- and endozoic fauna. 24 M. J. Grygier and K. Nomura

Marine Biology 26: 183-192. Fishelson, L. 1976 (dated 1973). Ecology of the crinoids of the northern Red Sea with emphasis on epi- and endozoic fauna associated with them. Journal of the Marine Biological Association of India 15(2): 461-473. Graff, L. von. 1887. Report on the Myzostomida collected during the Voyage of II.M.S. Challenger during the years 1873-76. Supplement. Report of the Scientific Results of the Voyage of H.M.S. Challenger During the Years 1873-76. Zoology 20(61): 1-16, Pis. I-IV. Grygier, M.J. 1994. Summary and significance of overlooked Japanese literature on Myzostomida. Proceedings of the Biological Society of Washington 107(1): 174-178. Hara, J. and Okada, Y. 1921. Two new species of Myzostomida. Annotationes Zoologicae Japonenses 10: 33-39. Jagersten, G. 1937. Myzostomiden von Prof. Dr. Sixten Bocks Expedition nach Japan und den Bonin-Inseln 1914. Arkiv for Zoologi 29A(17): 1-35, Pis. 1-2. Kogo, I. 1995. Crinoidea. Pp. 503-512. In: Nishimura, S. (Ed.) Guide to Seashore Animals ofJapan with Color Pictures and Keys, Vol. II. Hoikusha, Osaka. [In Japanese] Remscheid, E. 1918. Beitrage zur Kenntnis der Myzostomiden. Abhandlungcn Ilcrausgegeben von der Senckenbergischen Naturforschenden Gesellschaft 35(2): 179-225, Pis. XII-XIV. Rowe, F.W.E., Hoggett, A.K., Birtles, R.A. and Vail, L.L. 1986. Revision of some comasterid genera from Australia (Echinodermata, Crinoidea), with descriptions of two new genera and nine new species. Zoological Journal of the Linnean Society 86(3): 197-277. Uchida, II. 1992. Annelida. Pp. 310-373./«: Nishimura, S. (Ed.) Guide to Seashore Animals ofJapan with ColorPicturesand Keys, Vol. 1. Hoikusha, Osaka. [In Japanese] Wheeler, W.M. 1896. The sexual phases of Myzostoma. Mittheilungen aus dem Zoologischen Station zu Neapel 12: 227-302, Pis. 10-12.