Orobdella ghilarovi Nakano & Prozorova, 2019

Nakano, Takafumi & Prozorova, Larisa A., 2024, Terrestrial predatory leeches of the genus Orobdella (Hirudinea: Erpobdelliformes: Orobdellidae) endemic to the Southern Russian Far East: a new species of the genus from Primorsky Krai, Russia, Zootaxa 5424 (1), pp. 44-60 : 55-57

Orobdella ghilarovi Nakano & Prozorova, 2019

Figs 6 , 7

Orobdella whitmani Oka, 1895 — Ghilarov et al. (1969: 235–236, fig. 1)— Ghilarov & Perel (1971: table 1)— Lukin (1976: 464–466, figs 288, 289).

Orobdella ghilarovi Nakano & Prozorova, 2019, pp. 354–362 , figs 1–3— Prozorova (2019: 43, figs 1B)— Prozorova & Nakano (2020: 27, figs 1, 5).

Material examined. In total 17 leech specimens were examined. Russia • Primorsky Krai, Lazovsky Nature Reserve, near America Cordon; 43.25555°N, 134.03746°E; 5 Aug. 2019; Takafumi Nakano leg.; KUZ Z5024 • same collection data as for precedence; 43.25506°N, 134.03728°E ; KUZ Z5026 • same collection data as for precedence; 43.25475°N, 134.03731°E ; KUZ Z5030 • same collection data as for precedence; 43.25506°N, 134.03728°E ; Larisa Prozorova leg.; KUZ Z5027 – Z5029 • same collection data as for precedence; 43.25340°N, 134.03729°E ; Dmitry Ionutsa leg.; KUZ Z5031 • Primorsky Krai, Lazovsky Nature Reserve, near Zvoyzdochka Cordon ; 43.01640°N, 133.73036°E ; 7 Aug. 2019; Dmitry Ionutsa leg.; KUZ Z5032 – Z5034 • same collection data as for precedence; 43.01720°N, 133.72939°E ; KUZ Z5035 , Z5036 • same collection data as for precedence; 43.01739°N, 133.72946°E ; Takafumi Nakano and Dmitry Ionutsa leg.; KUZ Z5037 , Z5039 – Z5041 • same collection data as for precedence; 43.01741°N, 133.72958°E ; Takafumi Nakano leg.; KUZ Z5045 . Four specimens, KUZ Z5024 ( Fig. 6A–C ), Z5026, Z5030 and Z5032 were dissected .

Additionally, two cocoons ( Fig. 6D, E ) were collected. Russia • Primorsky Krai, Lazovsky Nature Reserve, near America Cordon ; 43.25576°N, 134.03758°E; 5 Aug. 2019; Takafumi Nakano leg.; KUZ Z5046 • same collection data as for precedence; 43.25488°N, 134.03717°E; Larisa Prozorova leg.; KUZ Z5047 .

Diagnosis (amended from Nakano & Prozorova 2019). Body length of mature individuals reaching ~ 6 cm. Somite IV uniannulate, somites VIII–XXV quadrannulate. Clitellum in somite XI b5 to somite XIII a2. Male gonopore slightly anterior to middle, or in middle of somite XI b5, female gonopore in middle of somite XIII a1, behind gastropore, gonopores separated by [(≥ 1/2)] + 4 + 1/2 annuli. Pharynx reaching to somite XIII b5–XIV a1.

Gastropore conspicuous, in middle of somite XIII a1. Gastroporal duct bulbous. Paired epididymides in somites XVI–XX, occupying nine to 12 annuli. Atrial cornua developed, ovate or ellipsoid.

Description. Measurements (mean ± 1SD, followed by ranges in parentheses; n = 17): BL 36.2 ± 8.6 mm (17.9– 49.5 mm), BW 3.4 ± 0.7 mm (2.0– 4.5 mm), CL 1.8 ± 0.3 mm (1.0– 2.3 mm), CW 2.1 ± 0.4 mm (1.2–2.7 mm).

Somites II–IV uniannulate ( Fig. 7A ). Somite V biannulate, (a1 + a2) = a3 ( Fig. 7A ). Somites VI and VII triannulate, a1 = a2 = a3 ( Fig. 7A ). Somites VIII–XXV quadrannulate, a1 = a2 = b5 = b6 ( Fig. 7A–C ). Somite XXVI bi-, or triannulate ( Fig. 7B ). Somite XXVII generally uniannulate ( Fig. 7B ), or rarely biannulate. Male gonopore slightly anterior to middle of somite XI b6 ( Fig. 7C ), or rarely middle of somite XI b6. Female gonopore in middle of somite XIII a1, located posterior to gastropore ( Fig. 7C ). Gonopores separated by [(≥ 1/2)] + 4 + 1/2 annuli ( Fig. 7C ).

Eyespots often in one pair on anterior margin of somite III, with two eyespots—one right-dorsolaterally and the other left-dorsolaterally—on posterior margin of somite V (a1 + a2) ( Fig. 7A ), or three pairs, 2nd and 3rd pairs dorsolaterally on posterior margin of somite V (a1 + a2). Nephridiopores in 17 pairs, each situated ventrally at posterior margin of a1 of each somite in somites VIII–XXIV ( Fig. 7C ).

Pharynx reaching to somite XIII b5–XIV a1 ( Fig. 7D ). Crop reaching to somite XIX b5–XIX/XX. Intestine reaching to somite XXIV a1/a2–a2/b5, with one pair of pouch-shaped intestinal ceca in somite XIX a2–XX a1 ( Fig. 7E ). Gastropore ventral, on middle of somite XIII a1 ( Fig. 7C ). Gastroporal duct bulbous, slightly winding at junction with gastropore, reaching to somite XIII/XIV–XIV a1 ( Fig. 7D ).

Testisacs multiple, in somite XX a2–XXI a1 to somite XXIV b6–XXV a2 ( Fig. 7F ); on right side, in total ~18– 25 testisacs; on left side, in total ~20 or ~25 testisacs. Paired epididymides in somite XVII a1–XVIII a1 to somite XIX b5–XX b5, occupying nine to 12 annuli ( Fig. 7F ). Paired ejaculatory ducts in somite XI b5 to somite XVII a1–XVIII a1 ( Fig. 7F ); coiled in position posterior to ovisacs; each duct loosely coiled, or nearly straight in position anterior to ovisacs. Pair of muscular atrial cornua developed, ovate, or ellipsoid in somite XI b5 and b6 ( Fig. 7F ). Atrium in somite XI b5 and b6. Paired ovisacs in somite XIII a2 and b5, right or left oviduct crossing ventrally beneath nerve cord; both oviducts converging into common oviduct in somite XIII a2 ( Fig. 7F ).

Coloration. In life, dorsal surface brown or grayish blue ( Fig. 6C ); ventral surface grayish or bluish gray. Color faded in preservative; dark mid-dorsal line rarely present from somite VIII b5–X a1 to somite XXIII b6–XXVII.

Cocoon. Ellipsoid, consisting of an inner capsule and outer layer ( Fig. 6D, E ); inner capsule, yellowish, major axis length 2.6 or 3.1 mm, minor axis length 1.9 or 2.1 mm; outer layer translucent, composed of coarse and irregular polyhedral cells, thickness ~ 0.3–0.6 mm; number of embryos uncountable.

Distribution and natural history. This species may be indigenous to forest habitats at the southernmost part of the Sikhote-Alin mountain range according to previous records ( Ghilarov et al. 1969; Ghilarov & Perel 1971; Nakano & Prozorova 2019) and its present occurrence at the LNR. The leeches were found curled up under rocks or fallen leaves in the forest during the daytime. Given the fact that mature individuals (KUZ Z5024 and Z5032) bearing a clitellum as well as cocoons were collected on 5 and 7 August 2019, the reproductive season of the Lazovsky population of O. ghilarovi may be around August, as estimated with the population at Anisimovka ( Nakano & Prozorova 2019). Orobdella ghilarovi deposits its cocoon under a stone or fallen leaves on the moist forest floor.

Remarks. The small Orobdella specimens from the LNR clearly belong to O. ghilarovi based on the possession of the following characteristics ( Nakano & Prozorova 2019): somite IV uniannulate, somites VIII–XXV quadrannulate, female gonopore and gastropore in middle of somite XIII a1, bulbous gastroporal duct, and epididymides occupying ~10 annuli. Our inferred phylogeny also corroborates the taxonomic identity of the LNR small-type specimens as O. ghilarovi . The O. ghilarovi holotype and paratypes possess a male gonopore at the middle of somite XI b5 ( Nakano & Prozorova 2019), but nonetheless, most of the LNR specimens bear a gonopore that opens slightly anterior to the middle of somite XI b6. Therefore, the diagnosis of this species is herein amended from that originally provided by Nakano & Prozorova (2019).

The COI genetic distances ( Table 2 ) calculated between the holotype and the LNR specimens (6.1% or 6.2%; or 6.1%–7.8% including the cocoon) are higher than the known divergence calculated between the quadrannulate sister species, O. kanaekoikeae Nakano and O. brachyepididymides Nakano (3.6%–4.6%; Nakano 2017b). Orobdella kanaekoikeae and O. brachyepididymides are well-differentiated from each other in morphological features, but nonetheless, the LNR specimens could not be unequivocally distinguished from the Anisimovka specimens by morphological characteristics. High intraspecific COI divergences were previously reported in the quadrannulate O. koikei [Kimura-2 parameter (K2P) distance, 4.8%–8.1%; Nakano 2012] and O. masasakikuroiwai (K2P distance, 0.5%–6.7%; Nakano 2014). In this study, therefore, we conclude that the LNR specimens belong to O. ghilarovi .

Figures

FIGURE 6. Orobdella ghilarovi, from Lazovsky Nature Reserve, Russia, mature individual (A–C: KUZ Z5024), and cocoons (D: KUZ Z5046; E: KUZ Z5047). A. Dorsal view. B. Ventral view. C. Dorsal view of live animal. D, E. Observe views of cocoons preserved in ethanol before dissection. Scale bars: 5 mm (A–C; same bar for A, B), 1 mm (D, E).

FIGURE 7. Orobdella ghilarovi, from Lazovsky Nature Reserve, Russia, mature individual (KUZ Z5024). A. Dorsal view of somites I–VIII. B. Dorsal view of somites XXIV–XXVII and caudal sucker. C. Ventral view of somites X–XIII. D. Ventral view of gastropore and female gonopore. E. Ventral view of junction between crop and intestine with intestinal ceca. F. Dorsal view of reproductive system, including ventral nervous system. Scale bars: 1 mm (A, D, E), 2 mm (B, C), 2.5 mm (F).