Cirrodrilus makinoi (Yamaguchi, 1934)

Ohtaka, Akifumi, Konno, Tomoaki & Gelder, Stuart R., 2024, Taxonomic Revision of Cirrodrilus makinoi (Annelida: Clitellata: Branchiobdellida) with a Redescription of C. homodontus, Species Diversity 29 (1), pp. 43-51 : 45-47

Cirrodrilus makinoi ( Yamaguchi, 1934) [Japanese name: Hime-zariganimimizu ( Yamaguchi 1935a)] ( Figs 2–4 )

Stephanodrilus (Stephanodrilus) makinoi Yamaguchi, 1934: 201, fig. 10, pl. 13, fig. 5; Yamaguchi 1935a: 24, fig. 12–2; Yamaguchi 1935b: 14, fig. 4C.

Stephanodrilus makinoi : Yamaguchi 1954: 102.

Cirrodrilus makinoi : Timm 1991: 329, fig. 46; Gelder 1996: 658; Gelder and Ohtaka 2002: 338; Ohtaka 2010: 460; Gelder 2019: 489; Ohtaka et al. 2020: 160.

Cirrodrilus tsugarensis Gelder and Ohtaka, 2000: 634 , fig. 1; Ohtaka 2010: 460; Ohtaka and Gelder 2015: 70, fig. 3D–F; Gelder 2019: 489; Ohtaka et al. 2023: 27, figs 3, 4J. syn. nov.

Type material. Yamaguchi (1934) did not designate any type specimens for C. makinoi . Six whole-mounted specimens identified in the ICHUM collection ( Gelder and Ohtaka 2002) were thus deemed to be syntypes for C. makinoi by Ohtaka et al. (2020), but these slide-mounted specimens had no labels and the catalogue information is believed lost. According to Yamaguchi (1934), therefore, the type locality of this species can be determined as somewhere, i.e., “Soranuma, Hattaribetsu, Shimofurano, Makomanai, Muroran, [or] Shintoku ,” in Hokkaido.

Material examined. All six syntype specimens of C . makinoi mentioned above: ICHUM-1402, 1404–1406, 1408, 1409. ICHUM-8591, a whole-mounted specimen of C. makinoi from Samani, Hokkaido (42.11°N, 142.99°E; No. 9 in Fig. 1 ), 2 October 2020, coll. T. Konno. ICHUM-8592 , a whole-mounted specimen of C. makinoi from Esashi , Hokkaido (45.05°N, 142.50°E; No. 8), 18 October 2020, coll. T. Konno. ICHUM-8593 , a whole-mounted specimen of C. tsugarensis from Jōzankei, Sapporo , Hokkaido (42.96°N, 141.22°E; No. 7), 31 August 2016, coll. A. Ohtaka and I. Koizumi. ICHUM-8594–8596 and an additional 15 whole-mounted specimens from Imabetsu, Aomori Prefecture, where is the type locality of C. tsugarensis (41.22°N, 140.56°E; No. 6), 9 September 1997, 14 November 1997, 24 October 2010, 28 October 2017, coll. A. Ohtaka. All the specimens were removed from Ca . japonicus.

Description. Body terete to pyriform, 2.0 to 3.0 mm long alive, 1.0– 1.5 mm preserved ( Fig. 2A ). Dorsal segmental appendage absent. Anterior nephridial pores opening separately onto the dorso-lateral surface of segment 3. Head slightly broader than segment 1 and posterior attachment disc. Peristomium shorter than head, and almost as wide as segment 1. Peristomium with five tentacles on dorsal lip, three pairs of lateral tentacles and small ventral lip ( Fig. 2B ). Among five dorsal tentacles, median one sometimes slightly shorter than others. Lateral tentacles slightly shorter than dorsal tentacles. Ventral lip with a medial emargination and with or without a pair of small lobes laterally. Dorsal and ventral jaws similar in shape and size, 23.0–35.0 µm wide at the base, each with large medial tooth on the anterior margin and two to four pairs of small lateral teeth on anterior surface ( Fig. 2C ); dental formula from 7/6 (3-1-3/2-1-3) to 8/8 (4-1-4/4-1-4). Small teeth pointed, each with angular ridge parallel to the median axes ( Fig. 2D ); the median pair of small teeth located at base of large median tooth, smaller than lateral small teeth. Most male reproductive organs located in segment 6 ( Fig. 2E ). Glandular atrium tubular, convoluted, consisted of dilated ental and slender ectal parts, total length 1.5–2.0 times segment diameter. Muscular atrium tubular, as thick as ectal part of glandular atrium, length about half segment diameter. Bursa ovoid, about quarter segment diameter. Spermatheca located in segment 5 ( Fig. 2E ), length 1.0–1.3 times segment diameter; ovoid spermathecal bulb, without ental process and tubular duct with dilated ental half.

Variations. Although five dorsal tentacles and three pairs of lateral tentacles on the peristomium were found in the specimens examined, length of their tentacles varied considerably. According to the original description of C. makinoi by Yamaguchi (1934), among five dorsal tentacles four are paired and sub-equal in length and slightly longer than the median one ( Fig. 3A ). The shorter median tentacle was found in the syntype ICHUM-1402 ( Fig. 3B ) as well as topotypes of C. tsugarensis from Imabetsu ( Fig. 3E ). On the other hand, five dorsal tentacles of subequal lengths were also encountered both in syntypes (ICHUM-1405, 1406; Fig. 3C, D ) and the Samani and Esashi specimens of C. makinoi and a specimen of C. tsugarensis from Sapporo ( Fig. 3F ). Lengths of the lateral tentacles, especially in the most ventral pair, are usually shorter than the dorsal ones. Size of the ventral lip varied, and when contracted a pair or a single lateral small lobe ( Fig. 3D ) may be visible, but usually they are absent ( Fig. 3F ). Similarly, the median emargination ranges from distinct (arrowed in Fig. 3A–E ) to almost indistinguishable ( Fig. 3F ).

Width of the dorsal and ventral jaws ranged from 26.0 µm to 29.0 µm (N = 8, mean value 27.1 µm) in the four syntype specimens of C . makinoi (ICHUM-1402, 1406, 1408, 1409). Those in the newly collected specimens of C . makinoi from Samani and Esashi , Hokkaido ranged from 27.0 µm to 32.0 µm, those in the specimen of C . tsugarensis from Sapporo , Hokkaido, were 30.0 µm and 32.0 µm, and the 18 topotypes of C . tsugarensis from Imabetsu, Honshu , ranged from 23.0 µm to 35.0 µm (N = 35, mean value 27.9 µm). Yamaguchi (1934: 202) drew a jaw and gave its magnification as ×440, and from the reprint fig. 10B in the work, its width was calculated, 34 µm wide. Although the calculated jaw width in the original figure ( Yamaguchi 1934) is slightly larger than those measured in the syntypes and other specimens from Hokkaido and Honshu localities, the difference is not significant.

The dental formula varies from 7/6 (3-1-3/2-1-3) to 9/9 (4-1-4/4-1-4). Although four pairs of lateral small teeth were drawn in the original figure ( Fig. 4A ) and found subsequently in our new material ( Fig. 4B ), jaws with fewer small teeth were observed more frequently. Twelve jaws in the six syntypes of C. makinoi showed a previously unreported variation in dental formula with a 3-1-3 arrangement ( Fig. 2C ) occurring most frequently in 7 jaws (58%), followed by four jaws with 4-1-3 (33%; Fig. 4C ). A unique arrangement of 2-2-2 ( Fig. 4D ) was found in a jaw in the syntype of C. makinoi (ICHUM-1404). In the 22 jaws in the 11 topotypes of C. tsugarensis from Imabetsu, Honshu, the dental formula with 3-1-3 ( Fig. 4E ) was the most frequently observed (16 jaws = 73%), followed by 3-1-2 ( Fig. 4F ) or 3-1-4 with three jaws of each arrangement (6 jaws = 27%).

Distribution. Yamaguchi (1934) reported under the name of Stephanodrilus (S.) makinoi (Nos 1–5 in Fig. 1 ) five localities on Hokkaido, while Gelder and Ohtaka (2000) and Ohtaka et al. (2023) recorded one each on Honshu (No. 6) and Hokkaido (No. 7) under the name of C. tsugarensis . Specimens used in the present study were collected from two additional localities on Hokkaido (Nos 8 and 9). In compiling these records, C. makinoi is shown to be widely distributed in Hokkaido along with an area on Honshu Island.

Host. Cambaroides japonicus (De Haan, 1841) , the “Japanese crayfish” or “Nihon-zarigani” in Japanese.

Habitat. Specimens have been observed alive on all parts of the exposed host’s surface.

Figures

Fig. 2. Cirrodrilus makinoi. A, Lateral view of a whole specimen, Yamaguchi (1934: fig. 10A) was redrawn; B, ventral view of peristomium, a whole-mounted specimen from Imabetsu; C, anterior view of the ventral jaw in whole-mounted syntype (ICHUM-1405) of C. makinoi; D, lateral view of the dorsal jaw in a whole-mounted specimen from Imabetsu; E, lateral view of segment 5 (left) with the spermatheca and male genitalia in segment 6 (right), a whole-mounted specimen from Imabetsu, Gelder and Ohtaka (2000: fig. 1E) was redrawn, scale bar=50µm. Abbreviations: b, bursa; ga, glandular atrium; ma, muscular atrium; mt, median tooth; sb, spermathecal bulb; sd, spermathecal duct; st, small tooth; vd, vas deferens. Scale bars: A, 200µm; B, E, 50µm; C, 10µm.

Fig. 3. Ventral views showing variations in the form of peristomia in Cirrodrilus makinoi, and including those of the junior synonym C. tsugarensis. A, Figure in the original description of C. makinoi, Yamaguchi (1934: fig. 10D) was redrawn; B–D, ICHUM-1402, 1405, 1406, syntypes of C. makinoi, whole-mounted specimens; E, a whole-mounted topotype of C. tsugarensis from Imabetsu; F, ICHUM-8593, a wholemounted specimen of C. tsugarensis from Sapporo, Ohtaka et al. (2023: fig. 3A) was redrawn. Downward and upward arrows indicate the position on the dorsal and ventral median lines, respectively. Scale bar: 50µm.

Fig. 4. Variations in the anterior views of jaws in Cirrodrilus makinoi, including those of the junior synonym C. tsugarensis. A, Original figure of C. makinoi, Yamaguchi (1934: fig. 10B) was redrawn; B, ICHUM-8591 from Samani; C, ICHUM-1404, a syntype of C. makinoi; D, another jaw in ICHUM-1404; E, ICHUM-8595, a topotype of C. tsugarensis from Imabetsu; F, another topotype of C. tsugarensis from Imabetsu. Scale bar: 10µm.

Fig. 1. Localities of Cirrodrilus makinoi (solid symbols) and C. homodontus (open symbols). Solid triangles, Yamaguchi’s (1934) records under the name of Stephanodrilus (S.) makinoi; solid discs, records under the name of C. tsugarensis in Gelder and Ohtaka (2000) for No. 6, and in Ohtaka et al. (2023) for No. 7; solid squares, locations of C. makinoi in the present study. Open star, location of Yamaguchi’s (1932b) specimens under the name of Cambarincola homodontus; open triangles, locations of Yamaguchi’s (1934) specimens under the name of S. (S.) homodontus; open circles, locations of C. homodontus in Ohtaka et al. (2023). 1, Oshamanbe; 2, Muroran; 3, Shimofurano; 4, Rubeshibe; 5, Shintoku; 6, Imabetsu; 7, Jōzankei, Sapporo; 8, Esashi; 9, Samani; 10, Soranuma; 11, Hattaribetsu;12, Sōya Cape; 13, Wakkanai; 14, Toikanbetsu; 15, Ōnuma; 16, Enbetsu, 17, Yagishiri Is.; 18, Teuri Is.; 19, Tomamae; 20, Sōunkyo; 21, Hamamasu; 22, Yoichi; 23, Otaru; 24, Kyōgoku; 25, Suttu; 26, Shimamaki; 27, Kuromatsunai; 28, Shikabe; 29, Hakodate; 30, Kaminokuni.