VENUS 69 (1–2):17–23, 2010 ©Malacological Society of Japan

A New Species of (Prosobranchia: ) Associated with Echinodiscus tenuissimus (Echinoidea: Astriclypeidae) from off Okinawa, Japan

Haruna Matsuda*, Daisuke Uyeno and Kazuya Nagasawa Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8528, Japan

Abstract: Hypermastus ryukyuensis n. sp. is described based on specimens from the clypeasteroid echinoid Echinodiscus tenuissimus caught at 10 m in depth in Oura Bay, Okinawa Prefecture, Japan. Of 30 currently valid species in the , H. tenuissimae, H. serratus and H. auritae resemble the new species, which is, however, distinguished from these three species by having a mucronate protoconch of nearly 2.5 whorls, apical teleoconch whorls abruptly increasing in diameter, indistinctly convex teleoconch whorls, a smaller and prosocline outer margin, which is not sinuate below the suture. In addition to the new species, H. peronellicola and H. tokunagai are known to occur in Japanese waters, and H. tenuissimae has been reported from E. tenuissimus from Thailand.

Keywords: new species, eulimid, parasitic gastropod, sand dollar,

Introduction

The genus Hypermastus Pilsbry, 1899 is a small group in the gastropod family Eulimidae that exclusively parasitizes irregular sea urchins (Warén & Crossland, 1991; Warén et al., 1994). In Japan, there are two valid species known in this genus, i.e. H. peronellicola (Kuroda & Habe, 1950) from Peronella japonica Mortensen, 1948 (Kuroda & Habe, 1950; Warén & Crossland, 1991; Matsuda et al., 2010) and H. tokunagai (Yokoyama, 1922) from Scaphechinus mirabilis A. Agassiz, 1863 (Yokoyama, 1922; Matsuda et al., 2008, 2010). Recently we found another Hypermastus species that is associated with the clypeasteroid echinoid Echinodiscus tenuissimus (L. Agassiz, 1847). Careful examination of the specimen, and comparison with other known taxa in the genus revealed that it represents an undescribed species, and it is described herein as new.

Materials and Methods

Five echinoids were collected by SCUBA on a sandy bottom at 10 m in depth in Oura Bay, Okinawa Prefecture, Japan, on 24 May 2008. They were brought to the laboratory and examined for parasitic gastropods. Ten eulimid gastropods were collected. Three and six specimens were first fixed in 70% ethanol and 10% formalin respectively, and all specimens were preserved in 70% ethanol. The remaining specimen was dried and coated with Pt for scanning electron microscopy (SEM). Nine specimens were observed using an Olympus SZX10 compound microscope and photographed with an Olympus DP20 digital camera. Six shell dimensions [shell length (SL), shell

* Corresponding author: [email protected] 18 H. Matsuda et al. width (SW), body whorl length (BL), aperture length (AL), aperture width (AW), and protoconch length (PL)] were measured from digital images using Adobe Photoshop®. Three dimensions of the outer lip margin [chord of the outer lip margin (distance from the posterior extremity to the anterior extremity of the outer lip margin: OL), length of protrusion of outer lip margin (distance from OL to the outer lip margin: LP), and distance from posterior extremity of the outer lip margin to widest point of LP (L)] of the shell were also measured (Matsuda et al., 2010: fig. 1D) because the shape of the outer lip margin is frequently considered as a taxonomically important character in eulimids (Warén, 1984; Bouchet & Warén, 1986). The shape of the protoconch and its imperceptible surface microsculpture were observed on a JEOL JSM–6390LV SEM. The nine specimens showed bimodality in shell length frequency, and they were separated into two groups: four small and five large specimens (Table 1). Since Hypermastus species are known to show sexual dimorphism, with males being significantly smaller than females, and some species were described based on larger female specimens (Warén & Crossland, 1991), we selected a large specimen, which is assumed to be a female, as the holotype. Drawings were made using a compound microscope and from photographs. Measurements were made for the holotype and eight paratypes (except the specimen used for SEM). Type specimens are deposited in the National Museum of Nature and Science, Tokyo (NSMT) and the University of the Ryukyus Museum (Fujukan), Okinawa (RUMF).

Results

Family Eulimidae Philippi, 1852 Genus Hypermastus Pilsbry, 1899 Hypermastus ryukyuensis n. sp. (Figs. 1; 2A–C, E)

Type material: Holotype, NSMT-Mo 76922 (Figs. 1, 2A-a, 2A-b); 6 paratypes, NSMT-Mo 76923–76928; 2 paratypes, RUMF-ZM 08521, 08522. All attached to the oral side of Echinodiscus tenuissimus (L. Agassiz, 1847), which was collected at a depth of 10 m in Oura Bay (26°54´N, 128°04´E) off Sedake, Nago, Okinawa-jima Island, North Pacific Ocean, Japan, 24 May, 2008. 1 paratype, NSMT-Mo 77012, 5.25 mm SL for SEM observation, ex oral side of E. tenuissimus, Oura Bay, 24 May, 2008. Description: Shell tall (e.g. 9.56 and 2.03 mm in SL and SW, respectively, for holotype; 5.04– 10.81 mm 1.30–2.20 mm for paratypes), slender, almost straight, and conical in form. Surface of shell white, translucent, smooth and highly polished. Protoconch distinctly set off, mucronate, consisting of nearly 2.5 whorls, ca. 0.27 mm long, separated by shallow but distinct incremental scar (Fig. 2B). Teleoconch comprises ca. ten whorls; first teleoconch whorl abruptly increasing in diameter. Body whorl constitutes almost two-fifths of shell length in holotype (BL/SL = 0.43). Side of each teleoconch whorl almost straight and indistinctly convex. Suture narrow, can be seen by reflected light. Incremental scars very thin and not conspicuously deepened, appearing on abapical whorls except body whorl, with intervals of 1.0–1.1 whorls, not aligned. Numerous incremental riblets regularly at suture, ca. 0.02 mm long and with intervals of ca. 0.04 mm (Fig. 2C). Aperture small, pear shaped, occupying almost one-fourth of shell length in holotype (AL/SL = 0.24), becoming narrower toward adapical end, its upper part constricted by slightly deflected outer lip margin. Columella-parietal wall forming weak angle. Outer lip margin slightly prosocline, curved with section above mid-point protruding in holotype (L/OL = 0.40). In live specimens, visceral mass visible through shell; purple in color with many scattered white spots (Fig. 2E). Eyes small, black, located on base of tentacles, visible through shell. not observed. New Species of Hypermastus from Japan 19 Total .2.5 - - - - ca .2.5 ca .2.5 0.26 0.25 0.21 0.20–0.21 0.26 0.25 0.260.41– 0.230.44 ±0.53 0.51 0.53 0.03 0.22– 0.460.24 ±0.30 0.29 0.30 0.05 0.26 ± 0.03 0.82–0.99 0.82 0.91 1.060.36–0.41 0.58 0.57 0.58 0.94 ± 0.07 0.46 ± 0.09 ca 56 5.04 5.24 5.04 9.89 –38 1.33 10.81 1.30 1.30 2.03 – 2.20 8.11 ± 2.70 1.77 ± 0.41 59 1.51 1.52 1.51 2.34 – 2.5091 0.90 0.83 0.83 1.28 – 2.0027 0.25 ± 0.26 1.480.25 0.27 0.45 –79 1.43 1.59 0.291.43 2.44 – 1.1628 0.20 ± 0.21 2.650.20 0.35 0.27 – 0.27 ± 0.43 0.01 2.12 ± 0.50 0.31 ± 0.09 .2.5 ca .2.5 10.6 7.4 10.6 6.6 6.6010.0 7.1 – 10.80 8.92 ± 1.74 ca .2.5 ca n. sp. .2.5 ca .2.5 ca Hypermastus ryukyuensis .2.5 ca 76922 76923 76924 76925 76926 76927 76928 08521 08522 Min – Max ± S.D. Mean Holotype Paratypes NSMT-Mo NSMT-Mo RUMF-ZM Shell dimensions for dimensions Shell No. teleoconch whorlNo. teleoconch 10.0 7.4 10.4 10.8 SW (mm)SW/SLBL (mm)BL/SLAL (mm)0.25 0.20 AL/SL 2.03 0.20 AW (mm)0.50 0.20 PL (mm) 0.41 0.21 0.26 4.10 1.36 OL (mm) 0.42 0.29 0.42 LP (mm) 0.22 2.15 0.43 0.50 2.26 2.65 0.23 L (mm) 2.15 0.23 L/OL 1.34 0.24 0.29 4.56 1.53 2.20 whorl No. protoconch 0.27 4.50 1. 2.50 0.89 2.41 4.37 0.51 0.34 2.43 0.29 1.40 2. 80 2.65 0.38 1.61 2.70 2.65 0.97 2.35 4.34 – 0.40 0.28 1.39 0.22 4.56 0.36 2.55 1. 0.40 0.54 1.48 0.26 0.86 3.63 0.38 2.63 ± 0. 0.28 0.89 0.92 0.43 2.65 0. 0.43 1.06 1. 0. 1.01 0.92 SL (mm) 9.56 5.33 10.81 10.79 10.73 5. Table 1. 20 H. Matsuda et al.

Fig. 1. Hypermastus ryukyuensis n. sp. Holotype (NSMT-Mo 76922), ventral view, 9.56 mm in shell length.

Morphometric variation: The nine specimens examined were divided by shell length into two distinct size groups (Table 1): one group is represented by large specimens, which are assumed to be females, and comprises the holotype (9.56 mm in SL) and four paratypes (NSMT-Mo 76924– 76926, RUMF-ZM 08522) (9.89–10.81 mm). The other group is made up of small specimens, which are assumed to be males, and comprises four paratypes (NSMT-Mo 76923, 76927–76928, RUMF-ZM 08521) (5.04–5.56 mm). A major variation can be recognized, especially in the proportions of some dimensions of the shell. The body whorl occupies approximately two-fifths of shell length in large specimens [BL/SL = 0.41–0.44 (n = 5)], but almost a half in small specimens [0.50–0.53 (n = 4)]. The aperture is also relatively smaller in large specimens [AL/SL = 0.22–0.24 (n = 5) vs. 0.29–0.30 (n = 4)]. Small specimens have a broader shell [SW/SL = 0.25– 0.26 (n = 4)] than large specimens [0.20–0.21 (n = 5)]. The outer lip margin of the shell is protruding above and below the mid-point in large [L/OL = 0.36–0.41 (n = 5)] and small [0.51– 0.58 (n = 4)] specimens, respectively. Infection rate: The five echinoids examined harbored a total of 10 individuals of H. ryukyuensis n. sp. The number of individuals per echinoid was not counted. Type locality: Oura Bay off Sedake, Nago, Okinawa-jima Island, North West-Pacific, Japan. Habitat: The new species was found attached to the oral side of its host, E. tenuissimus (Fig. 2D). A small and a large specimen frequently formed a pair (Fig. 2E). Some pairs were found keeping a distance from others on the same host. At each attachment site, a few spines were denuded and the surrounding area was slightly darker than the rest of the . Near the center of the attachment site, there was a single tiny hole (ca. 0.2 mm in diameter) formed by dissolution of the skeleton, probably caused by H. ryukyuensis n. sp. (Fig. 2F). Etymology: The specific name of the new species refers to its type locality, the Ryukyu New Species of Hypermastus from Japan 21

Fig. 2. Hypermastus ryukyuensis n. sp. and its host Echinodiscus tenuissimus. A. Holotype, NSMT-Mo 76922 (a–b, 9.56 mm in shell length) and paratype, NSMT-Mo 76923 (c–d, 5.33 mm). B. Scanning electron micrograph (SEM) of the protoconch. C. SEM of incremental scars and sutural incremental riblets. D. Aboral side of E. tenuissimus. E. A pair of H. ryukyuensis n. sp. attached to the host. F. SEM of two holes in the test of the host.

Islands. Remarks: The genus Hypermastus currently comprises 30 species, of which three, H. tenuissimae, H. serratus and H. auritae, are morphologically similar to the new species. H. tenuissimae is separated from H. ryukyuensis n. sp. by having 0.5–1.0 more whorls in the larval shell (length 0.4 mm), which is not mucronate. The profile of the outer lip margin in H. tenuissimae is orthocline and shallowly sinuate below the suture, while that of H. ryukyuensis n. sp. is prosocline and not sinuate. H. serratus is distinguished from the new species by the much more rapidly increasing diameter of its apical teleoconch whorls, more distinctly convex whorls, a more strongly convex profile of the outer lip margin, and a relatively larger aperture length/shell length ratio [AL/SL = 0.27 (based on Warén & Crossland, 1991: fig. 9A) vs. 0.24]. H. auritae differs from the new species by its larger shell, orthocline outer lip margin, and proportionally smaller body whorl [BL/SL = 0.36 (based on Warén & Crossland, 1991: fig 1G) vs. 0.43]. The new species clearly differs from the two Japanese species H. peronellicola and H. tokunagai in having a mucronate protoconch of nearly 2.5 whorls and numerous incremental riblets on the suture. 22 H. Matsuda et al.

Discussion

Eulimid gastropods are associated with hosts of a single class or a lower taxon (Warén, 1984). All species of Hypermastus whose hosts are known are parasites of irregular sea urchins (Warén, 1980; Warén & Crossland, 1991; Warén et al., 1994). This is supported by the fact that all three Japanese species of Hypermastus, including the present new species, occur on irregular sea urchins. The echinoid Echinodiscus tenuissimus is distributed in the Indo-West Pacific from the Red Sea to the Malayan Archipelago and from southern Japan to New Caledonia in the intertidal zone to a depth of approximately 20 m (Schultz, 2005). In Japan, this species has been reported only from the Satsunan and Ryukyu Islands (i.e. Tanegashima Island, Amami-Oshima Island and Okinawa-jima Island) (Mochizuki et al., 2008). In Okinawa-jima Island, E. tenuissimus was found only in Oura Bay, although many surveys were conducted by one of the authors (DU) for coastal marine invertebrates. This echinoid species is known to harbor H. tenuissimae in Thailand (Warén & Crossland, 1991) and H. ryukyuensis n. sp. is the second eulimid species from E. tenuissimus. It is desirable to study the geographical distribution of the two eulimid species in the Indo-West Pacific. In this study, narrow holes were found at the attachment sites in the test of E. tenuissimus. Many species of Hypermastus are known to make holes at attachment sites and feed on the host’s body fluid (Crossland et al., 1991; Warén & Crossland, 1991; Warén et al., 1994). The holes observed in this study are also likely to have been caused by H. ryukyuensis n. sp. which might have first dissolved its host’s test using some secretory material and then sucked the host’s body fluid. Among individuals of E. tenuissimus collected in this study, some were found uninfected but bearing scars. A similar observation has been made for several other species, e.g. H. mareticola and H. tokunagai (Warén et al., 1994; Matsuda et al., 2008). Crossland et al. (1991) also revealed in an aquarium that H. placentae is a temporary parasite because it could leave the hosts. Our observation of H. ryukyuensis n. sp. in the field indicates that the snail was easily detached from the host, which suggests that the new species is also a temporary parasite. Eulimids with separate sexes have a distinct sexual dimorphism, with males being 0.1–0.7 times smaller in shell length than females (Warén, 1984; Crossland et al., 1991; Warén & Crossland, 1991). H. ryukyuensis n. sp. perhaps shows a similar sexual dimorphism because the discontinuously smaller specimens (supposed males) were 0.6 times smaller on average than the larger ones (supposed females) and both were usually found in pairs. Further studies on the reproductive biology of the new species, including seasonal changes in sexual maturity and frequency of pairs, will be necessary to clarify this.

Acknowledgments

We thank Mr. Shin Nishihira for assistance in collecting samples. We are grateful to Mr. Takeshi Sasaki and Mr. Jun Nawa of the University of the Ryukyus Museum, for assistance and permission to use their laboratory facilities. We would like to thank Dr. Anders Warén of the Swedish Museum of Natural History for encouragement during the study. Thanks go to Dr. Shigeo Hori of the Hagi Museum, for valuable comments on the early version of the manuscript. Part of this work received financial support from Grants- in-Aid for JSPS Fellows (228067) to H. M. and from the Ocean Exposition Commemorative Park Management Foundation, Okinawa to K. N.

References

Bouchet, P. & Warén, A. 1986. Revision of the Northeast Atlantic bathyal and abyssal Aclididae, Eulimidae, Epitoniidae (, ). Bollettino Malacologico, Supplemento (2): 299–576. New Species of Hypermastus from Japan 23

Crossland, M. R., Alford, R. A. & Collins, J. D. 1991. Population dynamics of an ectoparasitic gastropod, Hypermastus sp. (Eulimidae), on the sand dollar, Arachnoides placenta (Echinoidea). Australian Journal of Marine and Freshwater Research 42: 69–76. Kuroda, T. & Habe, T. 1950. Eulimidae in Japan (I). Illustrated Catalogue of Japanese Shells 1(9): 53–60. Matsuda, H., Hamano, T., Yamamoto, K. & Hori, S. 2008. Ecological study of Hypermastus tokunagai (Gastropoda: Eulimidae), parasitic on the sand dollar Scaphechinus mirabilis (Echinoidea: Irregularia). Venus 66: 205–216. Matsuda, H., Hamano, T., Hori, S. & Nagasawa, K. 2010. Redescriptions and attachment modes of Hypermastus peronellicola and H. tokunagai (Prosobranchia: Eulimidae), ectoparasites on sand dollars (Echinodermata: Clypeasteroida) in Japanese waters. Venus 69: 25–39. Mochizuki, H., Mutoh, S., Yoshigou, H. & Ota, Y. 2008. The Clypeasteroida (Echinoidea: excluding for Fibulariidae) from shallow waters of the Ryukyu Islands in Japan, with notes for the Ryukyu’s Spatangoids. Miscellaneous Reports of the Hiwa Museum for Natural History (49): 77–101, pls. 1–9. (in Japanese with English abstract) Pilsbry, H. A. 1889. A new species of Australian . Proceedings of the Academy of Natural Sciences Philadelphia 51: 258. Schultz, H. 2005. Sea Urchins, A Guide to Worldwide Shallow Water Species. 484 pp. Heinke & Peter Schultz Partner Scientific Publications, Hemdingen. Warén, A. 1980. Descriptions of new taxa of Eulimidae (Mollusca, Prosobranchia), with notes on some previously described genera. Zoologica Scripta 9: 283–306. Warén, A. 1984. A generic revision of the family Eulimidae (Gastropoda: Prosobranchia). Journal of Molluscan Studies, Supplement (13): 1–96. Warén, A. & Crossland, M. R. 1991. Revision of Hypermastus Pilsbry, 1899 and Turveria Berry, 1956 (Gastropoda: Prosobranchia: Eulimidae), two genera parasitic on sand dollars. Records of the Australian Museum 43: 85–112. Warén, A., Norris, D. R. & Templado, J. 1994. Descriptions of four new eulimid gastropods parasitic on irregular sea urchins. Veliger 37: 141–154. Yokoyama, M. 1922. Fossils from the Upper Musashino of Kazusa and Shimosa. Journal of the College of Science, Imperial University, Tokyo 44: 1–200, pls. 1–17.

(Received March 16, 2010 / August 23, 2010)

沖縄県産フタツアナスカシカシパンから得られたハナゴウナ科 カシパンヤドリニナ属（新称）の 1新種

松田春菜・上野大輔・長澤和也

要 約

沖縄県大浦湾の砂底から採集されたフタツアナスカシカシパン Echinodiscus tenuissimusの腹面に見出 されたハナゴウナ類を Hypermastus ryukyuensis n. sp.フタツアナスカシカシパンヤドリニナ（新称）とし て記載した。カシパンヤドリニナ属には 30種が知られており，フタツアナスカシカシパンヤドリニナは インド西太平洋から報告された H. tenuissimae，H. serratus，H. auritaeに外形が似る。しかし，それらと は胎殻が約 2.5層で微突起状に突出し，後成殻から急激に幅が増大する点，螺層の側面がほぼ直線状で ある点，殻口が比較的小さく外唇縁が前方に傾き，縫合下で湾入することなく滑らかに湾曲する点で区 別できる。本種は大小の個体がペアでいることが多く，同属の他種のように大型個体が雌，小型個体が 雄と考えられる。日本には本種を含めてカシパンヤドリニナ属 3種が認められることになる。フタツア ナスカシカシパンからは同属の H. tenuissimaeが知られる。