80 VENUS 69 (1–2), 2010 ©Malacological Society of Japan

First Record of the Megadenus Rosén, 1910 (: ), Endoparasites of Sea Cucumbers, from Japan

Ryutaro Goto Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu-cho, Sakyo, Kyoto 606-8501, Japan; [email protected]

The gastropod family Eulimidae is characterised northward extension of the distribution of this genus by its parasitic associations with various in the Pacific. Based on field observations, (Warén, 1984). Megadenus Rosén, ecological data on this gastropod species are also 1910 is a genus of the Eulimidae that forms provided. endoparasitic associations with holothurians, although biological information on these snails is Material and Methods limited. Four species have been described in the genus, while additional collection records suggest I collected Stichopus chloronotus at Itton, Kasari the presence of two undescribed species (Warén, Bay, Amami-Oshima Island, southern Japan 1984). The type species of the genus, Megadenus (21°25´N, 129°36´E; Fig. 1A), during 26–29 May holothuricola Rosén, 1910, was described from 2009, and dissected them to search for endoparasitic specimens living in the respiratory tree of gastropods. Stichopus chloronotus is a common Holothuria mexicana Ludwig, 1875 in the Bahamas holothurian species living in shallow waters (Rosén, 1910). Humpreys and Lützen (1972) throughout the tropical Indo-West Pacific. If suggested that another Megadenus species had been gastropods were present, I recorded their number, collected from the respiratory trees of an position and posture in the holothurians. Before unidentified holothurian species in Luzon, the dissection, I measured the volume of the host Philippines, but it was assigned to the genus Stilifer holothurians using a graduated cylinder in the field. at that time and not described (von Martens, 1865). Megadenus voeltzkovi Schepman & Nierstrasz, 1913 Results and Discussion was described from the water-vascular ring of an unidentified holothurian (probably Holothuria Megadenus cantharelloides is the only known pardalis Selenka, 1867) in Zanzibar, East Africa eulimid living inside Stichopus chloronotus (Warén (Schepman & Nierstrasz, 1913), and an unnamed 1984), and can be distinguished from other Megadenus species was collected from the cloacal Megadenus species by the peculiar flange-like chambers of Holothuria atra Jaeger, 1833 in appendage of the proboscis (Humphreys & Lützen southeastern India (Jones & James, 1970; Mohan & 1972). The eulimid gastropods I collected from S. James, 2005). Megadenus cantharelloides chloronotus at Itton also had the flange-like Humpreys & Lützen, 1972 was described from the appendage of the proboscis, as well as the globose intestine of Stichopus chloronotus Brandt, 1835 in shell and body structure as described in Humphreys Aldabra, the Indian Ocean (Humpreys & Lützen, & Lützen (1972), and thus could be reliably 1972), and additional specimens of M. identified as M. cantharelloides. cantharelloides were collected more recently from Megadenus cantharelloides was found in three New Caledonia (Héros et al., 2007). Megadenus of 78 S. chloronotus holothurians, a parasitism rate oneirophantae Bouchet & Lützen, 1980 was of 3.8%. I also dissected three other sympatric described from the intestine of Oneirophanta holothurian species (Holothuria edulis Lesson, mutabilis Théel, 1879 in the deep sea of the 1830, Holothuria pardalis Selenka, 1867 and northeastern Atlantic (Bouchet & Lützen, 1980). Holothuria leucospilota Brandt, 1835) to search for These are all the known records of the genus. M. cantharelloides, but did not find any. The In this paper, I report the third record of M. numbers of gastropods in the three infested S. cantharelloides from Amami-Oshima Island, chloronotus were one, two, and three, respectively. southern Japan. This is the first record of the genus The solitary gastropod and two others from the Megadenus from Japan, and constitutes a significant second host (one small and one large placed close Short Notes 81

Fig. 1. Habitat and morphology of the endoparasitic gastropod Megadenus cantharelloides and its host holothurian Stichopus chloronotus. A. A gravelly tidal flat at Itton, Kasari Bay, Amami-Oshima Island. B, C, D. The internal organs of holothurians with pairs of endoparasitic gastropods (arrows) living at the base of the host respiratory trees. E. M. cantharelloides removed from the host. F. M. cantharelloides with flange of proboscis partly resected to show pseudopallium (broken line indicates the edge of the remaining flange). G. M. cantharelloides with the flange and pseudopallium resected. H. A dissected holothurian infested by two M. cantharelloides individuals (broken-lined boxes). Abbreviations: fp, flange of proboscis; i, intestine; pr, proboscis; ps, pseudopallium; rt, respiratory trees of the host holothurian; s, shell of gastropods. Scale: 1 cm (B, C, H), 1 mm (E, F, G), 2 mm (D). 82 VENUS 69 (1–2), 2010 together) were attached to the base of the respiratory holes were probably the feeding marks of the trees (Figs. 1B, C, D), as were one large and one endoparasitic gastropods. small specimens in the third holothurian. The In addition to M. cantharelloides, I found the remaining small one in the third host was positioned ectoparasitic eulimid gastropod Melanella acicula at a distance from the first two. Considering the Gould, 1849 on the body surface of six S. results of a previous study (Humpreys & Lützen, chloronotus (7.7%) and the pearl fish Encheliophis 1972), the larger individuals were probably females homei Richardson, 1844 in the digestive tube or and the smaller individuals males. respiratory tree of ten S. chloronotus (12.8%). The holotype of M. cantharelloides was collected Megadenus cantharelloides and the pearl fish were from the intestine of S. chloronotus (Humpreys & never found together inside the respiratory tree. Lützen, 1972). However, of the six M. Pearl fish were more frequently found in the cantharelloides I collected, five were attached to the holothurians with larger, rather than smaller, base of the respiratory tree connected to the volumes (Spearman’s rank correlation test: ρ = intestine, and one was attached to the middle of the 0.339, P = 0.002; Fig. 2), whereas M. cantharelloides respiratory tree. This may indicate that M. was found only in smaller holothurians (Fig. 2). cantharelloides can live in either the intestine or the Considering that E. homei feeds on small respiratory tree. The fragile, lustrous, globose shell such as fishes and crustaceans (Parmentier et al., (Figs. 1F, G) was embedded in the inner wall of the 1998), the low occurrence of gastropods in large S. host’s respiratory tree. The gastropods penetrated chloronotus may have been due to predation or the inner wall with their proboscis and protruded it disturbance by pearl fish. An alternative hypothesis into the coelom on the ventral side of the host (Figs. is that the small body size of the parasitised 1B, C, D, H). The proboscis is characterised by a holothurians was caused by a reduction in large umbrella-like flange (Fig. 1E). Under the nourishment due to snail infection. flange, a pseudopallium covers the shell, In this study, I found that M. cantharelloides has presumably to protect it from abrasion (Fig. 1F). a wide distribution throughout the Indo-West Humpreys & Lützen (1972) reported that the Pacific, maintaining high host specificity with S. gastropods of the same species extended the chloronotus. Because M. cantharelloides cannot proboscis from the intestine and fed on the inner move between hosts after settlement, high host side of the body wall of the host holothurian. In fact, specificity may increase the rate of encounter with I found several holes penetrating the ventral side of potential mates. This may be critical for the parasite the body wall of one parasitised holothurian. These because the rate of parasitism in Megadenus is

Fig. 2. Number of host holothurians Stichopus chloronotus in eight size classes, with their infestation status by endoparasitic gastropods Megadenus cantharelloides and pearl fish Encheliophis homei on Amami-Oshima Island. Short Notes 83 generally very low (Jones & James, 1970; this study). Perhaps the scarcity of records regarding this ナマコ類の内部寄生者である species is due to the very low rate of parasitism. An コノワタヤドリニナ属（新称） intensive search for holothurian endoparasites will （腹足綱：ハナゴウナ科） reveal whether the distribution of Megadenus is の日本初記録 much wider than previously thought.

References 後藤龍太郎

Bouchet, P. & Lützen, J. 1980. Deux gastéropodes 要 約 parasites d’une holothurie élasipode. Bulletin du Museum D’Historie Naturelle, Paris 2: 59–75. Héros, V., Lozouet, P., Maestrati, P., von Cosel, R., 奄美大島笠利湾の礫混じりの砂泥干潟に棲息す Brabant, D. & Bouchet, P. 2007. of るシカクナマコ Stichopus chloronotusの呼吸樹より New Caledonia. In: Payri, C. E. & Richer de ハナゴウナ科の一種 Megadenus cantharelloidesを記 Forges, B. (eds.), Compendium of Marine Species of New Caledonia. Documents 録した。本種は，インド洋のアルダブラに棲息す Scientifiques et Techniques 117, second るシカクナマコの消化管の内壁に寄生する個体に edition, pp. 199–254. IRD, Nouméa. 基づいて記載されたが，その後ニューカレドニア Humphreys, W. F. & Lützen, J. 1972. Studies on parasitic gastropods from echinoderms I. On で記録されて以来，報告がなかった。今回の報告 the structure and biology of the parasitic は M. cantharelloidesの世界三番目の産地であり， gastropod Megadenus cantharelloides n. sp., with comparisons on Paramegadenus n.g. Det Megadenus属の日本初記録でもある。本種の和名 Kongelige Danske Videnskabernes Selskab としてシカクナマココノワタヤドリニナを提案する。 Biologiske Skrifter 19: 1–27, pls. 1–4. 本記録により，シカクナマココノワタヤドリニナは Jones, S. & James, D. B. 1970. On a stiliferid gastropod parasitic in the cloacal chamber of インド洋からに日本にかけて広く分布し，その寄 Holothuria atra. Proceedings of the 主はシカクナマコのみであることが明らかになった。 Symposium on Mollusca, Marine Biological 2009年 5月に行った笠利湾での観察結果では，採 Association of India 3: 799–804. Mohan, M. K. R. & James, D. B. 2005. An incidence 集したシカクナマコの 4％にシカクナマココノワタ of parasitic infestation in Holothuria atra Jaeger. ヤドリニナが寄生しており，１ 匹のシカクナマコの SPC Beche-de-mer information Bulletin 22: 38. 呼吸樹から最大で 3個体が見つかる例も観察され Parmentier, E., Chardon, M., Poulicek, M., Bussers, J. C. & Vandewalle, P. Morphology of the た。 buccal apparatus and related structures in four species of Carapidae. Australian Journal of Zoology 46: 391–404. Rosén, N. 1910. Zur Kenntnis der parasitischen Schnecken. Lunds Universitets Årsskrift 6: 1–67. Schepman, M. M. & Nierstrasz, H. F. 1913. Parasitische und kommensalistische Mollusken aus Holothurien. Reise in Ostafrika in den Jahren 1903–1905 von professor Dr. Alfred Voeltzkow 4: 383–416. von Martens, K. E. 1865. Über die von Dr. Jagor gesammelte Stylifer-Arten von Luzon. In: Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin. 20 Juni 1865, p. 7. Warén, A. 1984. A generic revision of the family Eulimidae (Gastropoda, Prosobranchia). Journal of Molluscan Studies, Supplement (13): 1–96.

(Accepted August 22, 2010)