Willowsia Shoebotham, 1917

Cipola, Nikolas Gioia, Katz, Aron D., Bu, Yun & Godeiro, Nerivania Nunes, 2025, Systematics of Willowsia jacobsoni (Börner, 1913) (Collembola, Entomobryidae): morphology, postembryonic development, distribution, mitogenome and phylogeny, Zootaxa 5604 (3), pp. 201-233 : 206-211

Genus Willowsia Shoebotham, 1917

Willowsia jacobsoni ( Börner, 1913)

Figs 1–13 and Tables 2–3

Sira jacobsoni Börner, 1913: 49 , fig. 4, Java, Indonesia (orig. descr.)

Seira jacobsoni ; Salmon, 1964: 503 (comb.)

Willowsia jacobsoni ; Stach, 1965: 362

Synonyms:

Sira jacobsoni var. lipostropha Börner, 1913: 51 synonymized Zhang et al. 2011: 8.

Sira tricincta Schött, 1917: 31 synonymized by Womersley 1937a: 156.

Sira jacobsoni var. indica Handschin, 1929: 240 synonymized by Mari Mutt 1981: 370 (?).

Sira parajacobsoni Denis 1929: 105 synonymized by Denis 1941: 44.

Sira jacobsoni var. handschini Uchida, 1944: 4–5 synonymized by Mutt 1981: 370 (?).

Sira jacobsoni var. africana Delamare-Deboutteville 1950: 82 synonymized by Mari Mutt 1981: 370 (?). Willowsia mesothoraxa Nguyen, 2001: 25 synonymized by Zhang et al. 2011: 8.

Diagnosis. Adult specimens with violet pigment generally over most of the antennae, anterior dorsal margin of the head; females with Th II all pigmented; a dark blue transverse band formed by the posterior margin of Abd II and all Abd III and another dark blue band in Abd IV distally; coxae I–II with weakly pigments; femur III with a distal spot and tibiotarsus I–III with a median strip ( Figs 2–3 ). Scales lance-shaped, with interrupted ribs covering the proximal 1/3 or more (but not completely), present on head and trunk, absent on the appendages ( Fig. 6 ). Ant IV with a unilobed apical bulb ( Fig. 4A ). Dorsal chaetotaxy with 6 ‘An’, 4 ‘A’, 3 ‘M’, 4 ‘S’, 3 ‘Pa’, 4 ‘Pm’, 7 ‘Pp’ and 4 ‘Pe’ mac ( Fig. 9E ). Prelabral chaetae ciliate; labral p0–1 chaetae longer than the others ( Fig. 5A ); labral inner papillae with 4–5 projections and outer papillae with 3–4 projections ( Fig. 5B ); maxillary palp with 3 inner sublobal appendages; papilla E lateral process finger-shaped and almost reaching the base of the apical appendix; basolateral and basomedian labial fields with M, R, E, L1–2 ciliate, R smaller than the others ( Fig. 5A ). Th II a, m and p series with 2(a5–5i), 0 and 4(p1–3, p5) mac; Th III a, m and p series with 1(a6), 3(m5–7) and 4(p1–3, p6) mac ( Fig. 10E ); Abd I–IV macrochaetotaxy formula with 4, 2+1, 2+3, 3–4(5)+12–15 mac ( Figs 11E and 12E ); tenent hair ciliated and apically capitate; unguis basal teeth on the basal half, median tooth on distal 1/4 and smaller than the basal teeth, apical tooth on distal 1/8 and smaller than others; all unguiculus lamellae (ae, ai, pe, pi) smooth and acuminate, except for unguiculus III pe serrated ( Fig. 7A–B ); male genital plate papillate, with about 9+9 circumgenital chaetae; mucronal teeth subequal, spine surpassing the apex of the proximal tooth ( Fig. 7C ).

Remarks. Willowsia jacobsoni has been redescribed a few times throughout history, and in general its morphology was depicted similarly by different authors (e.g. Börner 1913; Schött 1917; Handschin 1925; Denis 1929; Mari Mutt 1981; Christiansen & Bellinger 1992; Nguyen 2001; Katz 2017). Even so, there are some differences listed by the previous authors that may be related to variations and/or interpretations, or even observational mistakes.

The specimens analyzed here, including the juveniles ( Figs 2–3 ), have the same color patterns and sexual dimorphism reported by Mari Mutt (1981) to specimens from Puerto Rico, except the depigmented Th III and the body completely pigmented. On labial posterior row, Mari Mutt reported the occasional presence of two extra chaetae (in basomedian field), and also illustrated (but did not report in his description) two smooth chaetae (L1–2) on basolateral field ( Mari Mutt 1981). However, in our analyzed specimens (including a few from Puerto Rico), no extra chaetae were observed, and L1 and L2 were always ciliated, so we do not know whether it could be a very atypical variation or an observational mistake.

The different interpretations (mac, mes or intermediate chaetae) can be considered in the Th. II dorsal chaetotaxy on to posterior row, with five mac reported by Mari Mutt (1981), four mac observed in our study ( Fig. 10E ), three mac depicted by Nguyen (2001), or two mac posteriorly seen by Katz (2017). The same happens in Th III, with three (p1–3) ( Fig. 10 ) or one (p3) inner mac, the latter being likely mistakenly described by Nguyen (2001). Katz (2017) considered one inner mac (m4) on Abd I, while other authors ( Mari Mutt 1981; Nguyen 2001), including the present work, considered three mac (m2–4) ( Fig. 11E ). On Abd IV, there may rarely be five inner mac ( Mari Mutt 1981), due to the intermediate size (mac or mes) of A3 chaeta ( Fig. 12E ), but the most common morphology varies between four or three (Sm absent) mac, the latter being a more frequent morphotype (e.g. Nguyen 2001). Still in Abd IV, other variations are revealed here for the first time, as three lateral mac (Fe2a2, Fe2, Fe2p), which were described as always present in Mari Mutt (1981). Concerning variable chaetae, on the head, three mac (p1e2, p2e2–e3) can also be present or absent. In addition, the S6 chaeta was not observed in Katz (2017), but is reported as mic or mac in Mari Mutt (1981). In the present work, S6 chaeta was observed as mac/mes only in the immature’s stages, except in 1 st instar ( Fig. 9 ).

The differences between the redescriptions herein reported for W. jacobsoni can influence comparisons (e.g., Katz 2017) and/or identifications, and consequently support descriptions of synonyms (e.g. W. parajacobsoni , W. mesothoraxa ). This subject has already been discussed before to other Entomobryidae (e.g. Viana et al. 2022, 2024). Once again, we reinforce caution in the interpretation, and consequently, in the diagnosis of Willowsia species.

Examined material. 1 female on slide ( INPA): Brazil, Amazonas, Manaus municipality, on laboratory benchtop in entomology department at the INPA, 03°05’42”S, 59°59’24”W, urban area, 82 m, 16.ii.2020, manual collect, NG Cipola coll. 2 males and 11 females on slides and 14 specimens in alcohol ( INPA): idem, except 12-15.iv.2021, JMC Nascimento coll. 9 specimens in alcohol ( INPA): Tarumã neighborhood, floating in the pool of the "Residencial Nascentes do Tarumã", 02°59’32”S, 60°02’09”W, urban area, 44 m, 05.i.2022, T Mahlmann coll. 1 female on slide ( INPA): Pará, Ananindeua municipality, urban area of “Águas Lindas” neighborhood, 01°23’24.4”S, 48°22’25.0”W, 31 m, 10-13.viii.2023, pitfall-trap, SS Viana coll. 8 specimens (1 male, 4 females and 3 undetermined) on slides ( INHS 148–810 ): USA, Puerto Rico, Aguada, Coloso Sugar Cane Mill, 18°22'52"N, 67°09'40", on sugar cane litter, 16-17.vi.1999, F. Soto-Adames coll. 1 male and 1 female on slides and 2 specimens in alcohol (20HN-SY7/ NJAU): China, Hainan Province, Sanya Bay, Sanya , 18°16’41.5”N, 109°29’02.2”E, 2 m ., 17.i.2020, D Yu coll. 2 males and 2 females on slides ( NUS): Singapore, National University of Singapore ( NUS), Kent Ridge campus, Lower Kent Ridge Rd , forest edge near University Hall building, 01°17’49.6”N, 103°46’35.7”E, Secondary tropical forest, Adinandra Belukar , 03.vi.2015, Malaise-trap, Maosheng Foo coll. 1 juvenile in 1 st instar, 4 juveniles in 2 nd instar, 2 juveniles in 3 rd instar, 3 juveniles in 4 th instar, 2 males and 11 females on slides and 82 specimens in alcohol ( NUS), plus 3 females on slides ( INPA): idem, except in Botany Department of the National University of Singapore, 01.xi.1990, HK Lua coll.

Geographical records ( Fig. 8 ). INDONESIA: Java, Samarang (= Semarang) (type locality) ( Börner 1913: 49); West Java, Tjibodas (actually Cibodas) ( Handschin 1925: 237); New Guinea (actually Papua, Indonesia), Cyclops Mountains ( Womersley 1937b: 205); Sumatra, Jambi Province ( Mawan et al. 2022: 5); Sumatra, Ranau and Wadi Kuala ( Handschin 1931: 481). PHILIPPINES: Luzon ( Gapud 1971: 14); Laguna, Mount Makiling ( Alviola et al. 2021: appendix). AUSTRALIA: North Queensland, Cedar Creek ( Schött 1917: 31); Victoria, Cumberland ( Womersley 1942: 28). PACIFIC OCEAN ISLANDS: Micronesia, Mariana and Caroline ( Uchida 1944: 4–5). JAPAN: Ogasawara, Marcus Island ( Uchida 1955: 203). CAMBODIA: Bokkor (= Bokor) ( Denis 1948: 240). VIETNAM: Nhatrang (= Nha trang) and DEo-Ca (= Cả Pass) ( DEnis 1948: 240); THái BìnH ( NGUYEn 2001: 25). NEPAL: Jumbesi and Maedane Karka ( Yosii 1966: 509). INDIA: West Bengal ( Mandal et al. 2024: 221). SRI LANKA ( Handschin 1929: 240). MADAGASCAR: Tamatave (= Toamasina) ( Denis 1929: 105). IVORY COAST ( Delamare-Deboutteville 1948: 316, 1950: 82, 1952: 73). USA: Maui and Oahu Islands ( Folsom 1932: 66; Christiansen & Bellinger 1992: 258). PUERTO RICO: Mayagüez ( Mari Mutt 1981: 367); Aguada ( Katz 2017: 552). TAIWAN: Taichung ( Lee & Park 1989: 275). CHINA: Hainan, Sanya Bay (new record). SINGAPORE: National University of Singapore (new record). BRAZIL: Amazonas, Pará states (new record).

Figures

FIGURE 1. Symbols used in the chaetotaxy descriptions of Willowsia jacobsoni.

FIGURE 2A–G. Willowsia jacobsoni, habitus of specimens from Singapore fixed in ethanol; A–E, dorsal view: A, 1st instar, B, 2nd instar, C, 3rd instar female, D, 4th instar male, E, adult female; F–G, lateral view: F, adult female, G, scanning electron microscopy. Scale bars: A–E (0.2 mm), F–G (0.5 mm).

FIGURE 3A–B. Willowsia jacobsoni, habitus of specimens from Brazil fixed in ethanol (dorsal view); A, female; B, male. Scale bars: 0.2 mm.

FIGURE 4A–B. Willowsia jacobsoni, SEM images of head; A, apex of Ant IV (distal view); B, lateral head, A–H represent the eyes (H partially covered by a scale), plus Ps2–5 and Pa3–8 series of the dorsal chaetotaxy. Scale bar: A (0.005 mm), B (0.05 mm).

FIGURE 5A–B. Willowsia jacobsoni, SEM images of head; A, anterior head, pl1–2 represent the prelabral chaetae, a1–2, m0–2 and p0–2 the labral chaetae, b.c. and t.a. of the maxillary palp, sb the appendages of sublobal plate (sb.4 omitted), A, B, C, D and E the labial papillae (arrow indicates right lateral process), a1–5, M, R, E and L1–2 the labial chaetae on basomedian and basolateral fields; B, labrum distally (anterior view), a1 is the anterior labral chaeta, white arrows indicate inner labral papillae and black arrow the outer labral papilla. Scale bars: A (0.02 mm), B (0.005 mm).

FIGURE 6A–D. Willowsia jacobsoni, SEM images of tergal structures; A–C, type II scales; D, Abd IV partial chaetotaxy (lateral view), B5 is a mac, T2 is a bothriotrichum, arrows indicate type II sensilla. Scale bars: A–C (0.005 mm), D (0.02 mm).

FIGURE 7A–C. Willowsia jacobsoni, SEM images of trunk appendages; A, distal tibiotarsus and empodial complex III (outer view), yellow arrows indicate the paired lateral teeth and red arrow the unpaired outer tooth; B, distal tibiotarsus and empodial complex III (anterior view), b.t., m.t. and a.t. are the unguis inner teeth, red arrow indicates the lateral outer tooth and white arrow the unguiculus lamellae; C, distal dens and mucro. Scale bar: A–C (0.01 mm).

FIGURE 8. Records of W. jacobsoni, star represents the type locality, red symbols previous records, and green symbols new records.

FIGURE 9A–E. Willowsia jacobsoni, development of dorsal head chaetotaxy; A, 1st instar; B, 2nd instar; C, 3rd instar; D, 4–5th instars, arrows indicate instar variation of chaetae as mac or mic; E, adult.

FIGURE 10A–E. Willowsia jacobsoni, development of dorsal Th II–III chaetotaxy; A, 1st instar; B, 2nd instar; C, 3rd instar; D, 4–5th instar; E, adult.

FIGURE 11A–E. Willowsia jacobsoni, development of dorsal Abd I–III chaetotaxy; A, 1st instar; B, 2nd instar; C, 3rd instar; D, 4–5th instars; E, adult.

FIGURE 12A–E. Willowsia jacobsoni, development of dorsal Abd IV–V chaetotaxy; A, 1st instar; B, 2nd instar; C, 3rd instar; D, 4–5th instars; E, adult; red arrows on Abd IV indicate secondary sensilla; p6 chaeta on Abd V is named as “ap6” by Szeptycki (1979) and Zhang et al. (2019).

FIGURE 13. Circular representation of the mitogenome of Willowsia jacobsoni. The innermost circle shows the GC content, the middle circle shows the reads coverage, and the outermost circle shows the gene features – rRNAs (purple), tRNAs (pink), and PCGs (green). (+) indicates the side of the major J-strand.