Howaia mogera (Yaginuma, 1972)

Ballarin, Francesco & Eguchi, Katsuyuki, 2023, Integrative taxonomic revision of the genera Nesticella and Howaia in Japan with the description of five new species (Araneae, Nesticidae, Nesticellini), ZooKeys 1174, pp. 219-272 : 219

Howaia mogera (Yaginuma, 1972)

Figs 1A-J , 4A-D , 15A , 16C, D (Japanese name: chibi-horahimegumoチビホラヒメグモ)

Nesticus terrestris Yaginuma 1970: 390, fig. 7 (♂, misidentification).

N. mogera Yaginuma 1972: 621, fig. 1 (♂♀); Yaginuma 1979: 275, pl. 6, figs 11, 12 (♂♀).

Howaia mogera Lehtinen and Saaristo 1980: 53, figs 7-9, 22-23, 29b (♂♀ transferred from Nesticus ).

Nesticus brevipes Paik 1996: 72, figs 1-10 (♀, misidentification).1

Type locality.

Japan, Tokyo Pref., Tamagawa.

Material examined.

Japan: Honshu Is.: Miyagi Pref.: 1♀, Tome-gun, Lake Izunuma, 20. July. 1986, A. Tanikawa leg. (MNHAH); 6♂, 4♀, Tamatukuri-gun , Naruko-cho , Myousada , 7-10.May.1996 , K. Kumada leg. (NMST-Ar.3587); Akita Pref.: 1♀, Akita-shi, Shimokitateyanagitate , Kagawa, 21.Nov.2005 , A. Fukushima leg. (NSMT-Ar.20405, identified as N. brevipes ); Yamagata Pref.: 1♀, Tsuruoka-shi, Oyama , 38.75628°N, 139.76331°E, 26.Aug.2019 , Y. Suzuki leg. (YSPC); Tochigi Pref.: 1♂ Tochigi-shi, Fujoka-machi, Uchino , Watarase-Yusuichi , 36.2353°N, 139.6574°E, Alt. : 20 m, 2.Apr.2022 , N. Kikuchi leg. (FBPC); Tokyo Pref.: 1♂ (holotype), Tamagawa , 3.Feb.1969 , H. Kobayashi leg. (NMST-Ar.73); 1♂, 2♀, Hachioji-shi, Minami-Osawa , Tokyo Metropolitan University campus, litter under bushes, 35.6245°N, 139.3863°E, 22.Sep.2020 , F. Ballarin leg. (FBPC); Hachijo-jima Is.: 3♂, 3♀, Okago, Hachijo Botanical Park , forest litter, 33.11044°N, 139.78432°E, 03.May.2021 , F. Ballarin leg. (FBPC); Kanagawa Pref.: 1♂, 2♀, Kawasaki-shi, Nakahara-ku, Kasugi-cho , Dec.1984 (exact date unknown) , H. Ono leg. (NMST-Ar.893); 2♀, Yokohama-shi, Maioka park, 6. July. 1986, A. Tanikawa leg. (MNHAH) ; Nagano Pref.: 2♀, Ueda-shi , 8.Sep.1998 , Y. Fujisawa leg. (NMST-Ar.6965); 3♀, Kamiina-gun, Ijima-cho , 35.67049°N, 137.91159°E, 09.Sep.2019 , Y. Suzuki leg. (YSPC); Shizuoka Pref.: 1♀ (Paratype), Tenryu-shi , Mar.1970 (exact date unknown) , H. Kobayashi leg. (NMST-Ar.74); 1♀, Hamamatsu-shi, Kita Ward, Inasacho Okuyama , 34.85102°N, 137.62569°E, under grass tuffs in a paddy field, 30.Sep.2019 , F. Ballarin leg. (FBPC); Fukui Pref: 1♀, Tsuruga-shi, Nagatani , under grass tuffs in a paddy field, 35.60836°N, 136.03872°E, 3.Oct.2019 , F. Ballarin leg. (FBPC); Mie Pref: 1♀, Iga-shi, Otani , under grass tuffs in a paddy field, 34.79919°N, 136.13501°E, 7.Oct.2019 , F. Ballarin leg. (FBPC); Kumamoto Pref.: 2♂, 1♀, Tamana-gun, Gyokutou-machi, Harakura , Yamakitasho-no-ana cave (山北小の穴), 20.May.1984 , T. Irie leg. (NMST-Ar.16065); Kagoshima Pref.: 1♀, Minami Kyushu-shi, Kawabe-cho , 26.Feb.2007 , K. Iohii (?) leg. (NMST-Ar.14585); Yakushima Is.: 1♂, Anbo , 207 m, broadleaf forest litter on a gentle slope 30.28458°N, 130.61799°E, 24.Sep.2021 , F. Ballarin leg. (FBPC); Suwanosejima Is.: 1♂, 2♀, Otohime-no-dokutsu cave, 8.Jul.2022, Y. Suzuki leg. (YSPC); Amami-Ōshima Is.: 1♂, Amami-shi, Kasarichō Ōaza Kise , 2 m, at the base of tufts of grass on a sandy seashore, 28.46221°N, 129.65013°E, 13.Jul.2021 , F. Ballarin leg. (FBPC); Okinawa Pref.: Okinawa-Honto Is.: 1♀, Naha-shi, Sueyoshi park, 70 m, humid broadleaves litter under trees, 26.22840°N, 127.71508°E, 21.Nov.2020 , F. Ballarin leg. (FBPC); 1♂, 4♀, Nakagami-gun, Yomitan-son, Namihira , Shimuku Gama cave (シムクガマ), Alt. : 72 m, large and long cave with a creek, 26.40242°N, 127.73125°E, 15.May.2022 , F. Ballarin leg. (FBPC); Aka-jima Is.: 3♀, 17.Mar.2022, Y. Suzuki leg. (YSPC); Kume-jima Is.: 1♂, Shimajiri-gun, Gima, Nameless Beach , under vegetation on a sandy seashore, 26.32681°N, 126.77002°E, Alt. : 3 m, 17.May.2022 , F. Ballarin leg. (FBPC); Miyako-jima Is.: 1♀, Nobaru Ueno, Pinza-Abu cave (ピンザアブ洞穴), 57 m, long and muddy cave, dark zone, 24.74853°N, 125.33443°E, 13.Nov.2020 , F. Ballarin leg. (FBPC); Ishigaki-jima Is.: 4♀, Tonoshiro, Fukubukuīzā Daiichi-do cave (フクブクイーザー第1洞), 66 m, long and humid cave with a small creek, 24.36533°N, 124.17721°E, 9.Nov.2020 , F. Ballarin leg. (FBPC); 4♀, same locality, 11.Nov.2020 , F. Ballarin leg. (FBPC); Yonaguni-jima Is.: 1♀, Irizaki , under stones in a meadow near the seashore, 24.44499°N, 122.9411°E, 30 m a.s.l., 4.Mar.2021 , F. Ballarin leg. (FBPC).

Diagnosis.

This species is closely related to H. alba sp. nov. and H. subterranea sp. nov. from which it can be easily distinguished by the presence of pigmentation and well-developed eyes (vs pigmentation and eyes lacking in both the other species) (Fig. 1H-J cf. Figs 2H-J , 3A-C ). Males of H. mogera can also be separated from males of H. alba sp. nov. by the thinner paracymbium (P) and the more squared and stockier distal process of paracymbium (Di) (vs wider P and longer and slightly sharper Di in H. alba sp. nov.) (Figs 1A, B, D , 4A-C cf. Figs 2A, B, D , 4E-G ). Females of H. mogera are distinguished from females of H. alba sp. nov. and H. subterranea sp. nov. by the shape of scapus (Sc), rectangular and with a flat posterior margin (vs stockier and larger Sc in H. alba sp. nov. or longer and distally dilatated Sc in H. subterranea sp. nov., both having a rounded posterior margin) (Figs 1E-G , 4D cf. Figs 2E-G , 3D, E , 4H , 13E ). See also Lin et al. (2016) for the diagnosis of H. mogera with other congeners of the same species group.

Redescription of male

(holotype). (redescription of habitus based on freshly collected specimen from Tokyo area due to the discoloration of the holotype). Habitus as in Fig. 1H . Total length. 1.94, Prosoma 1.10 long, 0.89 wide. Carapace rounded, yellowish with slightly darker striae. Cervical groove and fovea distinct. Eyes well developed. Eyes measurements: AME = 0.06, ALE = 0.09, PME = 0.09, PLE = 0.09, AME-ALE = 0.03, ALE-PLE = 0.00. Chelicerae, labium, maxillae, and sternum of same color as carapace. Legs uniformly yellowish. Legs measurements: I 5.07 (1.41, 0.43, 1.30, 1.24, 0.69), II 3.85 (1.10, 0.38, 0.90, 0.89, 0.58), III 3.26 (0.97, 0.33, 0.73, 0.73, 0.50), IV 4.44 (1.29, 0.40, 1.11, 1.06, 0.58). Opisthosoma uniformly dark grey with slightly lighter mark on antero-dorsal side.

Male palp as in Figs 1A-D , 4A-C . Cymbium relatively elongated, 3-4 robust spines on distal-prolateral margin (Fig. 1D ). Paracymbium with 1 distal (Di) and 1 ventral (Ve) processes. Distal process short, squared, and stocky, distinctly sclerotized. Ventral process sharp, spine-like, headed internally (Figs 1A-D , 4A-D ). Embolus (E) long and filiform, origin of embolus positioned at ~ 6:00 o’clock on radix (Rx). Radical apophysis (Ra) broad and dorsally flat with a granulate surface. Conductor with 3 distinct processes (Cp, Cr, Cm) and a half-transparent distal lobe (Cl). Prolateral process (Cp) flat and long, ribbon-like, headed counterclockwise, wrapped around the embolus. Retrolateral process of conductor (Cr) wide and thick, curved internally, with a broadened, flat central part. Median process of conductor (Cm) strongly sclerotized, short and stout, horn-like, ending with a blunt tip and having a smaller, stout ventral process (Figs 1A-C , 4A, B ).

Redescription of female

(based on specimen from Tokyo). Habitus as in Figs 1I , 15A . Total length: 2.44, Prosoma 1.19 long, 0.98 width. Cephalic area as in Fig. 1J . Carapace piriform. Eyes measurements: AME = 0.05, ALE = 0.08, PME = 0.08, PLE = 0.08, AME-ALE = 0.04, ALE-PLE = 0.01. Legs measurements: I 4.93 (1.42, 0.44, 1.28, 1.15, 0.64), II 3.96 (1.08, 0.39, 0.85, 0.78, 0.54), III 2.88 (0.86, 0.33, 0.63, 0.62, 0.44), IV 4.22 (1.30, 0.41, 1.10, 0.89, 0.52). Coloration and other details as in male.

Epigyne and vulva as in Figs 1E-G , 4D . Scapus (Sc) elongated antero-posteriorly, rectangular, slightly longer than wide, ending with a flat posterior margin (Figs 1E-G , 4D ). Copulatory opening (Co) at the inner-lateral sides of scapus. Internal ducts slightly visible through the transparent tegument, V-shaped. Copulatory ducts (Cd) straight, short, and thick, gradually diverging from each other, slightly coiled in the first half of the trait before reaching the spermathecae. Insemination ducts (Id) thin, coiled around the copulatory ducts. Spermathecae (S) small and rounded, separated from each other by ~ 1.5 their diameter (Fig. 1G ).

Size variation.

Male (based on 5 specimens): total length: 1.89-2.02, prosoma length: 0.84-1.07, prosoma width: 0.76-0.85. Female (based on 10 specimens): total length: 2.08-2.88, prosoma length: 0.96-1.15; prosoma width: female: 0.87-0.96.

Distribution.

East Asia (from South China to Korea and Japan). Introduced to Europe, Azerbaijan, and several oceanic islands (Hawaii, Fiji, Reunion, St. Helena, etc.). Although it is likely that H. mogera is naturally distributed in Asia, its precise center of origin, as well as the time and mode of its dispersion outside the Asian continent, are still unstudied. In Japan the species is widespread along the whole country in both mainland Japan and the Ryukyus (Fig. 16C, D ).

Habitat and ecology.

This species has a broad environmental tolerance. In Japan H. mogera can be found in a wide range of habitats, both natural and artificial, including caves, mines, artificial tunnels, small animal burrows, forest leaf litter, humid meadows, paddy fields, marshes, urban parks, greenhouses, vegetated seashores, coastal environments, etc. Howaia mogera usually builds simple scaffold webs in external habitats, under superficial stones, in empty spaces among the leaf litter or at the base of tufts of grass. Apparently, the populations living in mainland Japan are found less commonly in caves or cave-like habitats. In contrast, in addition to epigean environments, the populations living in the Ryukyu islands can be found more frequently in natural subterranean habitats, dwelling in both the twilight and dark areas of caves and tunnels.

Remarks on intraspecific variation.

Coloration and pattern of the opisthosoma can be rather variable, depending on the population or individual. Usually, populations living in mainland Japan show a darker habitus with an opisthosoma uniformly black or dark grey, sometimes having one or few small lighter marks on the dorsal side (Figs 1H, I , 15A ). Instead, individuals living in the Ryukyus seems to show a lighter pattern bearing several larger greyish dorsal marks, often merged together forming a continuous median stripe. Such pattern is shared by the southern Chinese populations (see Liu and Li 2013: fig. 18B). Legs are usually uniformly yellowish; however, some individuals show a faint darker annulation on the distal part of femur and tibia. The shape of scapus can also be slightly variable among individuals or populations, ranging from strongly rectangular to slightly inverted-trapezoidal or shorter and more squared, more rarely with strongly rounded distal margin (e.g., see Fig. 1E, F and Liu and Li 2013: fig. 18C, D). Yaginuma (1972: 620) illustrated a scapus with a strongly triangular shape for the paratype of H. mogera . Such extreme shape is abnormal and never observed by us in any of the examined specimens. In addition, the drawing by Yaginuma does not perfectly match with the shape of the scapus of the original sample (paratype NMST-Ar.74 from Tenryu-shi) which shows a normal rectangularly-shaped scapus.

Remarks on misidentifications.

Howaia mogera was initially misidentified by Yaginuma (1970) and described as the male of Nesticus (= Nesticella ) Nesticus terrestris based on a specimen from Tamagawa, Tokyo. Soon after Yaginuma recognized the mistake and described the species as new based on the same male together with a female specimen from Shizuoka ( Yaginuma 1972). Until now H. mogera has been recorded in several different countries and redescribed and illustrated numerous times by different authors ( World Spider Catalog 2023). However, these descriptions were all based on specimens collected far from the type locality, in different Asian countries (e.g., Korea: Kim et al. 1999, Kim and Lee 2018; China: Gong and Zhu 1982, Liu and Li 2013) or based on introduced populations (e.g., Fiji Is.: Lehtinen and Saaristo 1980; Hawaii Is.: Gertsch 1984; Azeirbaijan: Marusik and Guiseinov 2003; Poland: Bielak-Bielecki and Rozwalka 2011; Italy: Pantini et al. 2020). Herein, for the first time after the original description, we illustrate and redescribe the holotype and additional specimens from the type locality area.

In the past, the lack of information about the taxonomy of H. mogera , and in general on Nesticella species, has been the cause of misidentifications by senior arachnologists, sometimes confusing this species with other similar congeners. For example, the male of the blind H. mogera specimens from Miyako-jima Is. illustrated by Shimojana (1977) refers to the newly described H. alba sp. nov. Paik (1996) recorded Nesticus (= Nesticella ) Nesticus brevipes from South Korea based on female specimens. The illustrated samples do not match the morphology of this species (cf. Figs 5I, E-G , 7D and Paik 1996: figs 1-10) and probably they refer to more than one species of Nesticella or Howaia . Among them, the shape of epigyne and internal ducts of the specimens of the so-called groups A or B fits well with those of H. mogera ( Paik 1996: figs 6, 9, 10). Illustration of the female of H. mogera by Zhu and Zhang (2011: fig. 34A-C), clearly do not refer to this species, the illustrated epigyne and vulva being morphologically different from those found in the genus Howaia .

Remarks on phylogeny and biogeography.

Previous molecular analyses suggest that populations of H. mogera in Eastern Asia group into two well-distinct subclades with non-overlapping distribution, distributed respectively in North-Eastern Asia (= north clade) and South China (= south clade) ( Zhang and Li 2013; Ballarin and Li 2018; this work). In Japan both these two clades are apparently present. The north clade is distributed in mainland Japan covering the islands of Hokkaido, Honshu, Shikoku, and Kyushu. Its southernmost boundary seems to correspond to the island of Yakushima (Fig. 16C ). The south clade shares the same genetic pattern of the southern China populations (Fig. 14 ) and it is widespread along the whole Ryukyus and in the island of Hachijo-jima Is., south of Tokyo (Fig. 16C, D ). The presence of the south clade in Hachijo-jima Is., far away from the other known records, suggests a possible artificial introduction to this island. Some degrees of genetic difference (2.5-3.7%) and slight variations in the body pattern and habitat preference can be observed in populations belonging to the two clades (see remarks on habitat and variation discussed above). Nevertheless, no clear distinct morphological differences are observed in their genitalia. The result of our species delimitation analysis only partially supports them as two distinct species (Fig. 14 ). It is possible that they represent two cryptic species or, more likely, an early stage of species differentiation which is still in progress nowadays.

Figures

Figure 1. Howaia mogera A male palp (holotype), ventral view B same, retrolateral view C same, ventro-prolateral view D same, dorsal view E female epigyne ventral view (specimen from Tokyo area) F same after dissection, shape variation G vulva, dorsal view H habitus of male (specimen from Tokyo area) I habitus of female J cephalic area of female, frontal view. Abbreviations: Cd - copulatory duct; Co - copulatory opening; Id - insemination duct; S - spermatheca; Sc - scapus. Scale bars: 0.2 mm (A-G, J); 1.0 mm (H, I).

Figure 2. Howaia alba sp. nov. A male palp (holotype), ventral view B same, retrolateral view C same, ventro-prolateral view D same, dorsal view E female epigyne (one of the paratypes), ventral view F same, shape variation G vulva, dorsal view H habitus of male (holotype) I habitus of female (one of the paratypes) J cephalic area of female, frontal view. Abbreviations: Cd - copulatory duct; Co - copulatory opening; Id - insemination duct; S - spermatheca; Sc - scapus. Scale bars: 0.2 mm (A-G, J); 1.0 mm (H, I).

Figure 3. Howaia subterranea sp. nov. A habitus of female (holotype) B cephalic area of female, frontal view C habitus of female, lateral view D female epigyne, ventral view E vulva, dorsal view. Abbreviations: Cd - copulatory duct; Co - copulatory opening; Id - insemination duct; S - spermatheca; Sc - scapus. Scale bars: 1.0 mm (A, C); 0.2 mm (B, D, E).

Figure 4. Genitalia of Howaia mogera and H. alba sp. nov. A male palp of H. mogera, ventral view B same, retrolateral view C detail or paracymbium, dorsal view E female epigyne, ventral view E male palp of H. alba sp. nov., ventral view F same, retrolateral view C detail or paracymbium, dorsal view H female epigyne, ventral view. Abbreviations: Cl - lobe of conductor; Cm - median process of conductor; Co - copulatory opening; Cp - prolateral process of conductor; Cr - retrolateral process of conductor; Di - distal process of paracymbium; E - embolus; P - paracymbium; Ra - radical apophysis; Rx - radix; S - spermatheca; Sc - scapus; Sd - sperm duct; St - subtegulum; Te - tegulum; Ve - ventral process of paracymbium. Scale bars: 0.2 mm.

Figure 5. Nesticella brevipes A male palp (paratype), ventral view B same, retrolateral view C same, ventro-prolateral view D same, dorsal view E female epigyne (holotype), ventral view F same, female from Kyushu G vulva, dorsal view H habitus of male (old specimen from Kyushu); I habitus of female (specimen from Shikoku); J cephalic area of female, frontal view. Abbreviations: Cd - copulatory duct; Co - copulatory opening; Id - insemination duct; S - spermatheca; Sc - scapus. Scale bars: 0.2 mm (A-G, J); 1.0 mm (H, I).

Figure 7. Genitalia of Nesticella brevipes and N. terrestris A male palp of N. brevipes, ventral view B same, retrolateral view C detail or paracymbium, dorsal view E female epigyne, ventral view E male palp of N. terrestris, ventral view F same, retrolateral view C detail or paracymbium, dorsal view H female epigyne, ventral view. Abbreviations: Cl - lobe of conductor; Cm - median process of conductor; Co - copulatory opening; Cp - prolateral process of conductor; Cr - retrolateral process of conductor; Di I-II - distal process (es) I and II of paracymbium; Do - dorsal process of paracymbium; E - embolus; P - paracymbium; Ra - radical apophysis; Rx - radix; S - spermatheca; Sc - scapus; Sd - sperm duct; St - subtegulum; Te - tegulum; Ve I-II - ventral processes I and II of paracymbium. Scale bars: 0.2 mm.

Figure 13. Genitalia of Nesticella okinawaensis, Howaia subterranea sp. nov., and N. occulta sp. nov. A male palp of N. okinawaensis, ventral view B same, retrolateral view C detail or paracymbium, dorsal view D female epigyne, ventral view; E H. subterranea sp. nov., female epigyne, ventral view F N. occulta sp. nov. female epigyne, ventral view. Abbreviations: Ca - apophysis of the retrolateral process of conductor; Cl - lobe of conductor; Cm - median process of conductor; Co - copulatory opening; Cp - prolateral process of conductor; Cr - retrolateral process of conductor; Di I-II - distal processes I and II of paracymbium; E - embolus; P - paracymbium; Ra - radical apophysis; Rx - radix; S - spermatheca; Sc - scapus; Sd - sperm duct; St - subtegulum; Te - tegulum; Ve - ventral process of paracymbium. Scale bars: 0.2 mm.

Figure 14. Combined phylogenetic tree based on COI gene fragment reconstructed using maximum likelihood (ML) on RAxML and Bayesian inference (BI) on MrBayes. Support at each node denotes the ML bootstrap value (BV) and BI posterior probability (PP). Nodes highly supported by at least one method (BV ≥ 70 or PP ≥ 0.95) are highlighted by a black dot. Branch lengths were scaled concerning the number of substitutions per site. Each species corresponding to monophyletic clades are represented with different branch colors, species from Japan are highlighted with a colored background: red = H. mogera, azure = H. alba sp. nov., yellow = N. occulta sp. nov., violet = N. insulana sp. nov., light green = N. silvicola sp. nov., blue = N. brevipes, orange = N. terrestris, dark green = N. okinawaensis. The tree is rooted using the species Wraios longiembolus. The right lines denote the results of the species delimitation analysis based on morphological (MO) and molecular (ASAP, mPTP, and bPTP) data.

Figure 15. Nesticella and Howaia species in life and their natural habitats A female of H. mogera B female of N. terrestris C female of H. alba sp. nov. D female of N. occulta sp. nov. E female of N. okinawaensis F example of the epigean habitat of Nesticella species in the Ryukyus G habitat of H. alba sp nov. (dark zone of Tsuzupisuki-abu cave) H habitat of N. occulta sp. nov. (dark zone of Kabirano-ana cave) (all photos by F. Ballarin).

Figure 16. Distribution of Nesticella and Howaia species in mainland Japan and Ryukyu Archipelago A distribution of N. brevipes and N. terrestris in mainland Japan and neighboring countries B distribution of Nesticella and Howaia species endemic to the Ryukyu Archipelago C distribution of H. mogera in mainland Japan and neighboring countries D distribution of H. mogera in the Ryukyu Archipelago and neighboring countries. Colored squares refer to the type localities of the species, colored dots indicate the locations of specimens whose morphology has been checked during this study, dashed areas refer to the generally known distribution of the species, question marks refer to unclear distributions (see " remarks on misidentifications " of N. brevipes and N. terrestris).