Whitmania laevis ( Baird, 1869 )

Whitmania laevis ( Baird, 1869)

[Japanese name: Gohon-sesuzi-biru] ( Figs 1–3 View Fig View Fig View Fig )

Material examined. In total six specimens were collected from rice paddy located to the south of Mt. Kuburadake , Yonaguni Island, Ryukyu Islands, Japan on 19 March 2014 :

KUZ Z5159 View Materials , Z5160 View Materials , 24.45064°N, 122.95425°E, by Yoshiko Yamane; KUZ Z5161 View Materials – Z5164 View Materials , 24.44956°N, 122.95272°E, by Takafumi Nakano GoogleMaps . Three specimens, KUZ Z5159 View Materials , Z5162 View Materials , Z5164 View Materials , were dissected .

Description. Body firm, muscular, cephalic region small, from prostomium to somite XI with width increasing significantly in posterior direction, then from somite XII with constant width in posterior direction, ventrally flattened ( Figs 1A, B View Fig , 2A, C View Fig ). Oral sucker small, ovate, OL 1.4– 1.8 mm, OW 1.3–1.8 mm ( Figs 1B View Fig , 2C View Fig ). Caudal sucker ventral elliptic, CL 2.9–4.6 mm, CW 3.8–5.3 mm ( Figs 1B View Fig , 2G View Fig ).

Somite I completely merged with prostomium ( Fig. 2A View Fig ). Somite II uniannulate ( Fig. 2A View Fig ). Somite III uni- or biannulate, (a1 + a2) = a3, a3 sometimes with slight dorsal furrow ( Fig. 2A View Fig ). Somites IV and V generally biannulate, (a1 + a2) = a3, (a1+ a2) generally with slight dorsal furrow ( Fig. 2A, B View Fig ); somite V forming posterior margin of oral sucker ( Fig. 2C View Fig ). Somite VI dorsally triannulate, a1> a2 <a3, or a1 sometimes with obvious furrow, a1 (b1 = b2)> a2 <a3; ventrally biannulate, (a1 + a2)> a3 ( Fig. 2A–C View Fig ). Somite VII quadrannulate, a1> a2 = b5 = b6 ( Fig. 2A–C View Fig ), or sometimes a1 (b1= b2 dorsally)> a2 = b5 = b6. Somites VIII–XXIII quinquannulate, b1 = b2 = a2 = b5 = b6 ( Fig. 2A–E View Fig ). Somite XXIV quinquannulate, b1 = b2 = a2 = b5 = b6, or quadrannulate, b1 = b2 = a2 <a3 (b5 = b6) ( Fig. 2F, G View Fig ). Somite XXV quadrannulate, b1 = b2 = a2 = a3 ( Fig. 2F, G View Fig ). Somite XXVI biannulate, (a1 + a2)> a3, (a1 + a2) sometimes with slight furrow ( Fig. 2F View Fig ); (a1 + a2) being ventrally last complete annulus. Somite XXVII uniannulate ( Fig. 2F View Fig ). Anus at posterior margin of XXVII ( Fig. 2F View Fig ).

Male gonopore in anterior margin of, or middle of somite XI b6 ( Fig. 2D View Fig ). Female gonopore in anterior margin of somite XII b6 ( Fig. 2D View Fig ). Gonopores separated by ≤ 5 annuli ( Fig. 2D View Fig ).

Eyespots in 5 pairs, in parabolic arc ( Fig. 2A, B View Fig ); 1st pair on II; 2nd pair on III or III (a1 + a2); 3rd pair on IV (a1 + a2); 4th pair on V (a1+ a2); 5th pair on VI a2. Sensillae developed, 1 row on every annulus. Somital papillae developed, generally 6 papillae detected on a2 of each somite in VII–XXVII ( Fig. 2A, B, E, F View Fig ).

Nephridiopores in 17 pairs, one each situated ventrally at posterior margin of b2 of each somite in VIII–XXIV ( Fig. 2C, D, G View Fig ).

One median longitudinal furrow on ventral surface of oral sucker ( Fig. 2C View Fig ). Three rudimental jaws in oral cavity, 1 dorsal and 2 ventrolateral; salivary papillae undetectable; distichodont. Pharynx reaching to IX b2–b5. Crop reaching to XIX b2, giving rise to 1 pair of crop ceca (post-crop ceca)

in XIX b1–b2 to XX b5–XXII b2 ( Fig. 3A View Fig ). Terminal end of intestine forming sphincter between intestine and rectum, in XXI a2 to XXII b1–b5.

Testisacs in 9 or 10 pairs ( Fig. 3B View Fig ): 1st pair in XIII b5– b6 to XIV b2 (left testisac undetectable in KUZ Z5159); 2nd pair in XIV a2–b5 to XV b1; 3rd pair in XV a2–b5 to XVI b1; 4th pair in XVI a2–b5 to XVI b6–XVII b1; 5th pair in XVII a2–b6 to XVII b6–XVIII b2; 6th pair in XVIII a2–b5 to XVIII b6–XIX b1; 7th pair in XIX a2–b6 to XIX b6– XXb1; 8th pair in XX a2–b5 to XX b6–XXI b1; 9th pair in XXI a2–b6 to XXII b1–b2 (left testisac undetectable in KUZ Z5159); 10th pair (detected in KUZ Z5164 only) undeveloped, in XXII b5 and b6. Paired epididymides developed, globular or fusiform ( Fig. 3B, C View Fig ). Ejaculatory bulbs developed, elongated, fusiform ( Fig. 3B–D View Fig ); in large individuals (KUZ Z5159 and Z5162), in XI a2–XII b1 to XII a2–b6, occupying 6 or 7 annuli; in smaller individual (KUZ Z5164), in XI b5–b6 to XII b1–b2, occupying 4 annuli. Ejaculatory ducts narrow, running toward male atrium in XI a2–b5 to XII b2–XIII b5 ( Fig. 3B–D View Fig ); right duct crossing ventrally beneath nerve cord. Male atrium continuous with penis sheath ( Fig. 3B–D View Fig ). Penis sheath hook-like, U- or L-shaped, reaching to XIII b1–b6, then turning anteriorly to male gonopore ( Fig. 3B–D View Fig ).

Paired ovisacs ellipsoidal or globular, in XII b5–XIII b1 to XIII b1–b2 ( Fig. 3B, E, F View Fig ). Oviducts short ( Fig. 3B, E, F View Fig ); right oviduct crossing ventrally beneath nerve cord; both oviducts converging into common oviduct in XII b6 or XIII b2. Common oviduct thick, long, descending to female vagina in XII b6–XIII b2 to XIII b5–XIV a2 ( Fig. 3B, E, F View Fig ). Female vagina continuous to vaginal duct, tubular, in XII b6 to XIII b5–XIV a2 ( Fig. 3B, E, F View Fig ); vaginal cecum absent.

Coloration. In life, dorsal surface olive green with 5 discontinuous whitish-green longitudinal stripes, all stripes bordered in brown, each stripe fully or slightly faded on a2 of each mid-body somite ( Figs 1C View Fig , 2E View Fig ); several irregular black markings present on lateral margins; ventral surface tannish with black lateral margins, black markings present on lateral margins and caudal sucker, several irregular black markings also present on mid-ventral surface. Color faded in preservative, but longitudinal stripes and markings still present ( Figs 1A, B View Fig , 2G View Fig ).

Natural history. All individuals were found crawling in water of a paddy field at night.

Japanese name. The Japanese name “Gohon-sesuzi-biru,” which was proposed by Ohno (1998), is adopted herein. This name is likely to be derived from its five (= “gohon-”, Βψ) dorsal (= “-se-”, Ü) longitudinal stripes (= “-suzi”, ®); “biru” (or “hiru”) means a leech in Japanese.

Phylogenetic position and genetic distances. The ML (ln L = − 7516.22; not shown) and BI (ln L = − 7559.22; Fig. 4 View Fig ) trees had congruent topologies. The monophyly of each of the four Whitmania species was well supported: W. acranulata (BS =100%, PP = 1.0), W. edentula (BS = 100%, PP = 1.0), W. laevis (BS = 98%, PP = 1.0), and W. pigra (BS = 86%, PP = 0.98). Monophyly of three Whitmania species, i.e., W. pigra , W. laevis , and W. edentula , was well supported (BS = 94%, PP = 1.0). Whitmania laevis formed a monophyletic lineage with W. edentula (BS = 98%, PP = 1.0). The Taiwanese and Yonaguni W. laevis formed a distinct clade from the continental W. laevis sequences (BS = 89%, PP = 0.99).

The pairwise COI uncorrected p -distances between W. laevis and W. edentula were 10.5%–11.9%. The intraspecific COI variations within W. laevis were as follows: 0.2%–0.7% within the Taiwanese and Yonaguni populations; 2.1% between the Korean and continental Chinese sequences; and 1.8%–3.5% between the Taiwanese + Yonaguni and continental specimens.

Remarks. The Whitmania leeches collected from Yonaguni Island were identified as W. laevis based on the presence of the following characteristics, which were also reported by the prior studies ( Blanchard 1896; Moore 1927a; Yang 1996; Lai and Chen 2010): dorsal surface with five discontinuous whitish-green longitudinal stripes and several irregular black markings, ventral surface with black markings on lateral margins and caudal sucker; male gonopore at XI b6 and female gonopore at XII b6; paired epididymides globular or fusiform; penis sheath hook-like; oviducts short; common oviduct long, descending to female vagina; vaginal duct tubular; vaginal cecum absent. The results of our molecular analyses supported the taxonomic account of the Yonaguni Whitmania specimens determined by those morphological features. The results showed close genetic relationships between the Yonaguni and Taiwanese populations. This occurrence report provides the first record of W. laevis from the Ryukyu Islands (see Itoh 2003). It remains uncertain whether W. laevis on Yonaguni Island was introduced from Taiwan or anywhere else in recent years, but nonetheless, it is noteworthy that the Yonaguni specimens have unique COI sequences.

The large W. laevis specimens from Yonaguni Island possess nine pairs of testisacs. However, the Chinese and Taiwanese specimens had 11 pairs of testisacs ( Yang 1996; Lai and Chen 2010) and those from eastern India had 10 pairs of testisacs ( Moore 1927a). Although the small specimen (KUZ Z5164) possesses 10 pairs of testisacs, the last pair seemed to be rudimentary. The reduced number of testisac pairs may be a shared feature of the W. laevis population endemic to Yonaguni Island.

The present phylogenies revealed a sister relationship between W. laevis and W. edentula for the first time. This relationship is consistent with the morphological similarities in female genital organs between the two species ( Whitman 1886), both of which have a thick common oviduct directly descending to the vagina and a tubular vagina and vaginal duct. The calculated uncorrected p -distances between W. laevis and W. edentula were above 10%, and thus met the average interspecific variations detected among the hirudinid predatory species of Haemopis Savigny, 1822 ( Kvist et al. 2023). Therefore, W. laevis and W. edentula should both receive distinct species status within Whitmania . Three of the five Whitmania species, i.e., W. acranulata , W. edentula , and W. pigra , were originally described from Japan. Therefore, their topotypic DNA data and morphological features are essential to reveal the true species richness and evolutionary history of this predatory genus endemic to South and East Asia.