Gracilentulus europaeus Szeptycki, 1993

Nakamura, Osami, 2021, The Japanese species of the genus Gracilentulus (Protura: Acerentomidae), Zootaxa 4991 (2), pp. 271-294 : 286-292

Gracilentulus europaeus Szeptycki, 1993

Figs. 11–12 , Table 3

Gracilentulus europaeus: Szeptycki, 1993, pp. 383–384 , 390–392, Figs 4–8 , 18–31.- Szeptycki, 2007, p. 59.

Gracilentulus sp. Nakamura et al., 2011, p. 62.

Materials examined. 174 females, 39 maturi juniores, 39 larvae II, 1 larva I, botanical garden of Rishiri Town Museum, Senhoushi, Rishiri Island, Hokkaido, mixed forest of Picea jezoensis , Abies sachalinensis , Betula ermanii , Sorbus commixta , 45.113436º N, 141.216213º E, elev. 25 m, 18-X-2007, M. Sato leg.; 2 females, botanical garden of Hokkaido University, Chûô-ku, Sapporo, Hokkaido, grassland, 43.063456º N, 141.34378º E, elev. 20 m, 8-V- 1980, O. Nakamura leg.

10 specimens (three females (NSMT-Ap 561–563), three maturi juniores (NSMT-Ap 564–566), three Larvae II (NSMT-Ap 567–569), one Larva I (NSMT-Ap 570)) are deposited in NMST , 10 specimens (four females, three maturi juniores, three larvae II) in the collection of Rishiri Town Museum, and the remaining specimens in the collection of Saitama Museum of Natural History .

Diagnosis. Cephalic setae sd5 and d6 absent; foretarsal sensillum b’ posterior to α4, d at almost same level with t2; pore lt on abdominal tergite VII situated anteriorly to level of A5; abdominal tergites II–VI with eight anterior setae; anterior lines of abdominal sternites II–III continuous.

Description based on Japanese specimens. Body length 923 μm in extended condition. Head length 103–109 μm; width 70–76 μm; labrum short, 5–6 μm, LR = 17–20. Cephalic setae l3, l5, sd4 short setiform, 6–7 μm; sd5 and d6 absent; d7 and sd7 subequal length, 15–17 μm ( Fig. 11A ). Maxillary palpus with two sensilla on penultimate seg- ment, dorsal sensillum, 9 μm, slightly longer than ventral one, 7 μm ( Fig. 11B ). Labial palpus with three setae and one sensillum ( Fig. 11C ). Canal of maxillary gland simple ( Fig. 11D ), CF = 9–11. Pseudoculus circular or slightly broader than long ( Fig. 11E ), 7–9 μm x 9 μm, PR = 13–14. Pore fp present ( Fig. 11A ).

Foretarsus ( Figs. 11F, G ) 72–77 μm; claw 24–26 μm, TR = 2.9–3.1; empodium 3–4 μm, EU = 0.1–0.2. Dorsal sensillum t1 claviform, almost same level with α3, BS = 0.4–0.5; t2 thin, situated at same level with d; t3 small knob-like. Exterior sensillum a situated between γ1 and α3, its apex reaching base of f; b almost same length as c; c almost same level with α3; d situated at same level with t2; apices of a, b, c and d each reaching base of f; e situated posterior to α5; f at about halfway between e and g; g slightly distal to t3; apices of e, f and g surpassing tarsus. Interior sensillum a' broad, slightly posterior to t1, its apex surpassing base of b'; b' slightly distal to t2, its apex not reaching base of c'; c' at same level with α6, its apex surpassing tarsus. Single pore present near bases of c and t3, respectively. Setae β2 sensillum-like; δ1–5 short. Middle tarsus 33–35 μm, its claw 14–17 μm; hind tarsus 39–41 μm, its claw 17–18 μm.

Body chaetotaxy as in Table 3 and Figs. 12A–G . On thoracic tergites II–III ( Fig. 12A ), P1a and P2a short setiform; P1a halfway between P1 and P2; P2a slightly nearer to P3 than to P2; P5a rudimentary. 1 and 2 on thoracic tergite I 27–30 and 11–13 μm; P1, P1a and P2 on thoracic tergite II 20–25, 5–7 and 32–33 μm. Abdominal tergites II–VII with four pairs of anterior setae (A1, A2, A4, A5); but A1 on VII often asymmetrical absent ( Fig. 11B ); P3 on II–VI situated anterior to other posterior setae ( Fig. 11B ); P1a on I–VI absent; P2a and P4a on I–VII and P1a on VII short setae, about 1/4 of P 1 in length; P2a on II–VI nearer to P2 than to P3; on VII P1a nearer to P1 than to P2, P2a at middle between P2 and P3. Sternite VIII with a single row of four setae; P1a on sternites II–VI similar to dorsal ones; P1a on VII slightly longer than those on sternites II–VI. P1, P2 and accessory setae (P2a, P4a) on abdominal tergite VI 25–26, 30 and 6–7 μm; P1, P1a and P2 on VII 26–28, 6–7 and 28 μm; P1a on sternite VI 6–7 μm; one on VII 7–8 μm.

Thoracic tergite II–III with pore sl ( Fig. 11A ). Pore psm present on abdominal tergites I–VIII, those on VIII with accompanying teeth ( Fig. 11C ); al on V-VII ( Fig. 11B ); lt on VII ( Fig. 11G ). Sternite V with spsm; VI with two pairs of spsm; VII with spsm and spm ( Fig. 11G ).

Abdominal appendage II–III with two setae ( Fig. 11H ), apical seta, 5 μm, about 1/3 length of subapical one, 14–16 μm. On abdomen VIII, striate band developed, striae distinct ( Fig. 12C ); comb with about 9 teeth; scattered teeth present on anterior part ( Fig. 12C ). Anterior line on abdominal sternites II–III continuous ( Fig. 12D ). Female squama genitalis with stout pointed acrostylus ( Fig. 11I ).

Maturus junior: Body length 656 μm in extended condition. Head length 87–92 μm, width 61–65 μm, LR = 19–28; pseudoculus slightly longer than width or circular, 7 μm x 7–8 μm, PR = 12–14; CF = 10–11; pore fp often invisible. Foretarsus 62–65 μm; claw 21–23 μm, TR = 2.9–3.0; empodium 3–4 μm, EU = 0.1–0.2. Shape and posi- tion of foretarsal sensilla, and pores same as those of imago, BS = 0.4. Middle tarsus 25–28 μm, its claw 15–16 μm; hind tarsus 28–31μm, its claw 15–18 μm. Body porotaxy almost same as those of imago, but sl on thoracic tergites II–III often invisible; lt on abdomen VII missing. Scattered small teeth present on anterior part on abdomen VIII.

Larva II: Body length 611 μm in extended condition. Head length 77–86 μm, width 58–61 μm, LR = 26–32; pseudoculus slightly longer than width or circular, 6–7 μm x 7–8 μm, PR = 12–14; CF = 10–12; pore fp missing. Foretarsus 51–56 μm; claw 18–20 μm, TR = 2.7–3.0; empodium 3–4 μm, EU = 0.1–0.2. Foretarsal sensilla b’ missing, BS = 0.4–0.5; pores same as those of preceding stages. Middle tarsus 24–28 μm, its claw 13–15 μm; hind tarsus 26–30 μm, its claw 14–15 μm. Pore al present on abdominal tergites I–VII; psm on V–VIII, those on V asymmetric or invisible, those on VIII with accompanying teeth; spsm present on abdominal sternites V–VII, those on V often missing, those on VII often asymmetric.

Larva I: Body length 299 μm in compact condition. Head length 76 μm, width 49 μm; rostrum indistinct; pseudoculus slightly longer than width, 7 μm x 5 μm, PR = 12; CF = 12; pore fp absent. Foretarsus 42 μm; claw 18 μm, TR = 2.2; empodium 3 μm, EU = 0.2; BS = 0.4; sensilla b’ and c’ missing; pores absent. Pore psm present on abdominal tergites VII–VIII, those on VIII without accompanying teeth, a pair of ventral pore present at side on telson.

Chaetotaxic variation. The chaetotaxy is quite variable and more than one irregularity exists in many specimens. The following anomalies were recorded.

Imagines (176 specimens): thoracic tergite I— asymmetric presence of additional P1 (2 examples), asymmetric absence of P2a (1 ex.); thoracic sternite I, presence of additional Ac (2 exs.); thoracic sternite II—presence of additional ventral A2 (1 ex.); abdominal tergite I—symmetric presence of additional A2 (1 ex.); abdominal tergite II— absence of A1 (1 ex.), asymmetric absence of A2 (1 ex.), asymmetric presence of A3 (2 ex.), asymmetric absence of A4 (1 ex.), asymmetric presence of additional A5 (1 ex.), absence of P1 (1 ex.), absence of P2 (1 ex.), asymmetric absence of P2a (1 ex.); abdominal tergite III—asymmetric absence of A4 (5 exs.); abdominal tergite IV —asymmetric absence of A1 (1 ex.) ; abdominal tergite V —asymmetric presence of additional A1 (1 ex.) , asymmetric presence of A3 (1 ex.), asymmetric absence of A4 (5 exs.), asymmetric absence of P2 (1 ex.); abdominal tergite VI —asymmetric absence of A2 (1 ex.) , asymmetric presence of A3 (1 ex.), asymmetric absence of A4 (4 exs.), asymmetric absence of P1 and P2 (1 ex.); abdominal tergite VII —asymmetric absence of A1 (158 exs.) , asymmetric absence of A2 (2 exs.), asymmetric presence of A3 (5 exs.); abdominal tergite VIII—absence of M1 (1 ex.), presence of Mc instead of M1 (4 exs.), presence of Mc (1 ex.), asymmetric absence of M2 (1 ex.); abdominal tergite IX—asymmetric absence of 1 (1 ex.), asymmetric presence of additional 1 (1 ex.); abdominal segment X—asymmetric presence of additional 1 (1 ex.); abdominal sternite III—presence of one seta lateroposterior to Ac (2 exs.); abdominal sternite IV —asymmetric presence of A1 (6 exs.) , presence of one seta lateroposterior to Ac (1 ex.), asymmetric presence of P1 (1 ex.); abdominal sternite V —asymmetric presence of A1 (3 exs.) , presence of A1 instead of Ac (1 ex.); abdominal sternite VI —asymmetric absence of P3 (1 ex.) ; abdominal sternite VII —presence of one seta between A2 and P2 (1 ex.) , asymmetric absence of P1a (1 ex.); abdominal sternite VIII—presence of 5 setae (30 exs.) and 6 setae (1 ex.); abdominal sternite X—asymmetric absence of seta 1 (1 ex.).

Maturi juniores (39 specimens): abdominal tergite II—asymmetric presence of A4 (1 ex.); abdominal tergite III—asymmetric absence of A1 (2 exs.), asymmetric absence of A2 (1 ex.): abdominal tergite V —asymmetric absence of A1 (1 ex.) , asymmetric presence of A4 (1 ex.); abdominal tergite VII —asymmetric (37 exs.) and symmetric (2 exs.) absence of A1, asymmetric (18 exs.) and symmetric (2 exs.) presence of A2, asymmetric absence of A4 (1 ex.); abdominal tergite VII —absence of Mc (1 ex.) ; abdominal sternite IV —asymmetric absence of P1 (1 ex.) .

Larvae II (39 specimens): abdominal sternite II—absence of Pc (1 ex.); abdominal sternite III— absence of Pc (1 ex.); abdominal sternite VIII—asymmetric absence of seta 1 (1 ex.).

Notes. Although the Japanese specimens differ slightly from the original description in the length of foretarsal sensilla b and d (neither apex reaching the base of f in the original description) along with b’ (its apex reaching the base of α 6 in the original description), and in the chaetotaxy of abdominal sternite I in larva II (A2 absent in the original description). However, these differences represent intraspecific variation. Indeed, there are no substantial differences in the important specific features from the original description. This Gracilentulus species belongs to the “ gracilis ” group, which is recorded from Japan for the first time here.

Szeptycki (1993) described the anterior setae on abdominal tergite VII as seven setae (Ac, A 2, A4, and A5). Since A 1 setae emerge in the maturus junior, their occurrence was confirmed in 176 females and 39 maturi juniores obtained in the current study. In further analysis, a pair of A1 setae appeared in 18 females while one A1 had disappeared with high frequency ( Table 4 ) .

When one A1 disappeared, the remaining A1 was found to move slightly toward the center. Hence, seta Ac in Szeptycki (1993) should be A1; thus, the anterior setae on abdominal tergite VII should be assigned as eight setae in pairs of A1, A2, A4, and A5, although A1 disappears asymmetrically with high frequency.

Szeptycki (1993) suggested the possibility of facultative parthenogenesis in G. europaeus . In the present study, 176 adults from two sites were all females. Additionally, at Rishiri Island, all larval stages except for prelarva were obtained, indicating that an alternation of generations is taking place here. This result supports the hypothesis of Szeptycki (1993).

Both localities from which the species was obtained in Hokkaido were artificial botanical gardens. In Rishiri Island, surveys were conducted at several sites, including natural forests, but the species was only collected in a botanical garden ( Maehara et al. 2003; Nakamura et al. 2011). Although proturans have been collected from more than 560 localities in the main island of Hokkaido ( Imadaté & Ohnishi 1993), Gracilentulus species had previously not been obtained. Indeed, the current record from the botanical garden in Sapporo is the only locality at which collection has been successful on the main island of Hokkaido. These results suggest that this species was probably introduced into Hokkaido. Similar examples of out-of-country introduction were reported for Proturentomon minimum (Berlese) and Gracilentulus gracilis (Berlese) in New Zealand by Tuxen (1985). In addition, as stated by Minor (2008), the fact that only females were found is also indicative of out-of-country introduction.

Distribution. Europe ( Poland, France, and Portugal), USA (Delaware), new to Japan (Hokkaido).

Figures

FIGURE 4. Gracilentulus microtrichus sp. nov., holotype (NSMT-Ap 560). A) head, dorsal view; B) sensilla on maxillary palpus; C) labial palpus; D) canal of maxillary gland; E) pseudoculus; F) abdominal appendage II; G) comb on abdominal tergite VIII; H) female squama genitalis.Arrow shows a pore.Abbreviations: fp, frontal pore; D, dorsal sensillum; V, ventral sensillum. Scale bar: 10 μm.

FIGURE 5. Gracilentulus microtrichus sp. nov., holotype (NSMT-Ap 560). A) foretarsus, exterior view; B) foretarsus, interior view; C) sensillum t3. Arrows show pores. Scale bars: A–B, 20 μm; C, 5 μm.

FIGURE 6. Gracilentulus microtrichus sp. nov., holotype (NSMT-Ap 560). A) dorsal view of thoraces I–II, left side; B) dorsal view of posterior part of thorax III, left side; C) sensilla P1a and P2a on thoraces; D) thoracic sternite I; E) thoracic sternite II. Abbreviations: sl, sublateral pore. Scale bars: C, 5μm; 20 μm for other images.

FIGURE 7. Gracilentulus microtrichus sp. nov., holotype (NSMT-Ap 560).A) dorsal view abdominal segment V, right side; B) dorsal view of abdominal segments VI–VII, right side; C) dorsal view of abdominal segments VIII, right side; D) ventral view of abdominal segments V–VII, right side.Abbreviations: al, anterolateral pore; lt, laterotergal pore; psm, posterosubmedial pore; spsm, sternal posterosubmedial pore. Scale bar: 20 μm.

FIGURE 8. Gracilentulus aokii Imadaté, holotype (NSMT-Ap 78). A) head, dorsal view; B) dorsal view of maxillary palpus; C) ventral view of maxillary palpus. Arrow indicates a pore. Abbreviation: fp, frontal pore. Scale bars: 20 μm for A, 10 μm for B–C.

FIGURE 11. Gracilentulus europaeus Szeptycki from Rishiri Is., Hokkaido. A) head, dorsal view; B) maxillary palpus; C) labial palpus; D) canal of maxillary gland; E) pseudoculus; F) exterior view of foretarsus; G) interior view of foretarsus; H) abdominal appendage II; I) female squama genitalis. A–G, female (NSMT-Ap 561), H–I, female (NSMT-Ap 562). Abbreviations: fp, frontal pore; D, dorsal sensillum; V, ventral sensillum. Arrows indicate pores. Scale bars: 20 μm for A, F, G; 10 μm for other images.

FIGURE 12. Gracilentulus europaeus Szeptycki from Rishiri Is., Hokkaido.A) dorsal view of thoraces I–II, left side; B) dorsal view of abdominal segments V–VII, right side; C) dorsal view of abdominal segment VIII, left side; D) abdominal sternites II–III; E) posterior part of abdominal sternite V; F) ventral view of abdominal segment VI; G) ventral view of abdominal segment VII. A, E–G, female (NSMT-Ap 561); B, D, female (NSMT-Ap 563); C, female (NSMT-Ap 562). Abbreviations: al, anterolateral pore; lt, laterotergal pore; psm, posterosubmedial pore; sl, sublateral pore; spsm, sternal posterosubmedial pore. Scale bar: 20 μm.