Pilophorus hyotan, Yasunaga & Duwal & Nakatani, 2020

Yasunaga, Tomohide, Duwal, Ram Keshari & Nakatani, Yukinobu, 2021, Reclassification of the plant bug genus Pilophorus in Japan and key to the genera and species of Japanese Pilophorini (Hemiptera: Heteroptera: Miridae Phylinae), Zootaxa 4942 (1), pp. 1-40 : 12-16

Pilophorus hyotan n. sp.

( Figs 3 A–F, 4A–H, 7A, C, E, 8, 9A–E, I–K, 10A–B, 15A–I, 16A–F, M–O)

Pilophorus sp. Yasunaga, 1997: 32 (faunal list, fig., Japanese name).

Pilophorus typicus (nec Distant): Duwal et al., 2014: 270 (diag.).

Type material. Holotype (♂). JAPAN: Kyushu: Nagasaki Pref., Nagasaki City, Kabashima Island, 32.555222, 129.777022 [ Fig. 8B , 1 ], Persicaria thunbergii (Sieb. & Zucc.) H. Gross ex Nakai , 29 Sep 2019, T. Yasunaga ( NIAES) ( AMNH _PBI 00380666). Paratypes. JAPAN: Kyushu: Same data as for holotype 1 ♂, 3 ♀; same locality and collector, 32.555333, 129.776688, male flowers of Mallotus japonicus , 15 Jun 2013, 1 ♂ and 24 Aug 2013 1 ♂ ( TYCN); Nagasaki City, Mieda, 32.820444, 129.732700 [ Fig. 8B , 4 ], engine vacuum netting, 31 Jul 2018, T. Yasunaga et al., 3 ♂, 2 ♀ ( TYCN); same data except for date, 11 Feb 2020, 2 ♂, 1 ♀ ( TYCN); same data, except for date 10 Oct 2020, 1 ♂ ( TYCN); same data, 5th instar nymph when collected and emerging on 18–20 Feb 2020, mating on 14 Mar, dead on 17 Mar, 1 ♂ ( TYCN); same data, 5th instar nymph when collected and emerged on 20 Feb 2020, mating on 14 Mar, dead on 29 Apr, 1 ♀ ( TYCN); same data, except for date 23 May 2020, 4 ♂, 1 ♀ ( TYCN); same data, dead on 11 Jun after reared, 1 ♀ ( TYCN); same data, except for date 16 Jun 2020, 2 ♂, 4 ♀ ( TYCN); same data, except for date 14 Nov. 2020, 7 ♂, 1 ♀ ( AMNH, CNC, TYCN); same locality, hatching on 27 Mar 2020 (oviposited egg in lab.), emerging on 7 May and dead on 13 Mar, 1 ♂ ( TYCN); same locality (reared in lab.), May– Sep 2020, NWHS Biology Club, 10 ♂, 6 ♀ ( TYCN); Nagasaki City, Taira, Odorise, 32.814570, 129.778477 [ Fig. 8B , 5 ], engine vacuum netting, 4 Aug 2018, T. Yasunaga, 1 ♂, 1 ♀ ( TYCN); Nagasaki City, Ohama, Inasayama Park, 32.7588, 129.8470 [ Fig. 8B , 7 ], Artemisia sp., 7 Aug 2020, NWHS Biol. Club, 2 ♂ ( TYCN); same locality, 9 Oct 2020, H. Tabuchi, 1 ♂ ( NWHS); Nagasaki City, Yotsue, Agri-Hills Park, 32.809585, 129.797100 [ Fig. 8B , 6 ], male flowers of Mallotus japonicus , 15 Jun 2019, T. Yasunaga, 1 ♂ ( TYCN); Nagasaki City, Kinkai-Tonehara, 32.900745, 129.794545 [ Fig. 8B , 3 ], engine vacuum netting, 10 Oct 2020, T. Yasunaga, 5 ♂, 3 ♀ (1♀ dead on Dec 6 after reared) ( TYCN); Nagasaki City, Nishi-umi Town, 32.865440, 129.791285, Artemisia sp., 25 Oct 2020, T. Yasunaga, 1 ♀ (dead on Dec 7 after reared) ( TYCN); Nagasaki City, Kohno’ura, 32.8788, 129.6957 [ Fig. 8B , 2 ], Pueraria lobata leaves, 2–4 Aug 1996, T. Yasunaga, 3 ♀; Nagasaki Pref., Isahaya City, Takaki Town, Todoroki Valley, 32.95, 130.11, Artemisia sp., 3 Jun 2002, T. Yasunaga, 2 ♂; Isahaya City, Shirakimine, 32.92407, 130.06854, flowers of Humulus japonicus , 27 Sep 2014, T. Yasunaga, 2 ♂; Tsushima Island, Tsushima City, Izuhara Town, Hiyoshi, 34.209555, 129.291200, Artemisia sp., 21 Jul 2020, H. Asanabe, 1 ♂, 1 ♀ ( TYCN) ( AMNH _PBI 00380667); same data, except for date 4 Aug 2020, 1 ♂, 1 ♀ ( TYCN); Tsushima City, Izuhara Town, Isaribi Park, 34.2055, 129.2985, Artemisia sp., 24 Jul 2020, H. Asanabe, 1 ♂ ( TYCN); Fukuoka Pref., Kurume City, Mii-machi, 33.3060, 130.5471, flowers of white clover, 24 Jun 1992, T. Yasunaga, 1 ♀ ( TYCN); Kumamoto Pref., Aso-gun, Oguni Town, 33.12, 131.07, 15 Sep 2020, H. Tabuchi, 1 ♂ ( TYCN); Kagoshima Pref., Kouyama Town (= current Kimotsuki Town), 31.33, 130.95, 28 Aug 1992, T. Yasunaga, 1 ♂ ( TYCN). Shikoku: Ehime Pref., Suwazaki Park, 33.4433, 132.3985, planted azaleas, 20 Sep 1992, T. Yasunaga, 3 ♂, 1 ♀ ( TYCN); Kochi Pref., Same’ura-dam, 33.755, 133.548, 22 Aug 1998, M. Takai, 1 ♂, 1 ♀ ( TYCN); Kochi Pref., Cape Muroto, 33.29, 134.17, 27 May 1997, I. Yamashita, 1 ♂ ( TYCN) (00380668). Honshu: Fukui Pref., Tsuruga City, Naka-ikemi, 35.656 136.089, 22 Jun 1994, T. Kishimoto, 1 ♂ ( TYCN); Hyogo Pref., Takasago City, Kitawaki, 34.791, 134.753, 1 Sep 2002, T. Nozaki, 1♂ ( TYCN); Ohya Town, Miyagaki, 18 Sep 1997, Y. Nakatani, 1 ♂ ( NIAES); Ibaraki Pref., Tsuchi’ura City, Shishitsuka, 36.081381, 140.164382, Artemisia sp., 16 Jun 2000, Y. Nakatani, 2 ♂, 4 ♀ ( NIAES) (00380669); Okayama Pref., Hiruzen, 35.309, 133.639, flowers of Humulus japonicus , 4 Sep 2002, T. Yasunaga, 1 ♂ ( TYCN); Okayama City, Kanayama, 34.744, 133.939, on chrysanthemum, 3 Oct 1992, T. Yasunaga & K. Nagai, 2 ♂ ( TYCN); Osaka Pref., Minoo City, Shimotodoromi, 27 Jun 1993, Y. Nakatani, 1 ♂ ( NIAES); Tokyo, Univ. of Tokyo Komaba Campus, 35.66006, 139. 68521, 22 Jun – 21 Oct 2013, T. Ishikawa, 1 ♂, 4 ♀ ( TUAK); Tokyo, Hachijo Island, Kohno Minato, 33.11, 139.81, 6 Aug 1948, M. Kubota, 1 ♀ ( NIAES); same data except for date 9 Aug 1948, 1 ♂, 1 ♀ ( NIAES); Hachijo Island, 33.12, 139.78, 21–22 Sep 1982, H. Hasegawa, 1 ♂, 1 ♀ ( NIAES). Additional material examined. JAPAN: Kyushu, Nagasaki City, Wakimisaki, engine vacuum netting, 2 Jun 2019, NWHS Biol. Club, 1 ♀ ( NWHS); Nagasaki City, Nameshi 2- chome, 32.8105, 129.8408 [ Fig. 8B , 9 ], flowers of Humulus japonicus Sieb. & Zucc. (Cannabaceae) , 25 Sep 2014, T. Yasunaga, 1 ♀ ( TYCN). Ryukyus: Ishigaki Island, Sokobaru-dam, 24.430556, 124.211667, Y. Nakatani, 17 Mar 2012, 1 ♂ ( NIAES); Ishigaki Island, Ban’na Park, 24.383, 124.173, Hirado-Azalea ( Rhododendron x pulchrum ), 4 Mar 1998, T. Yasunaga, 1 ♂ ( TYCN); Iriomote Island, Monbanari (=Monbanare), 24.295777, 123.872638, 20 Mar 2007, Y. Nakatani, 3 ♂, 5 ♀ ( NIAES). KOREA: Chungcheongbuk-do: Cheongwon-gun, Nami-myeon, Sudae-ri, 7 Jun 2008, S.W. Park, 1 ♂ ( SNU); Cheongwon-gun, Naesu-eup, Deokam-ri, 22 Jun 2008, S.W. Park; 5♂ ( SNU). Chuncheongnam-do: Cheonan-si, Susin-myeon, Baekja-ri, 5 Oct 2008, S.W. Park, 1 ♀ ( SNU). Gyeongsangbukdo: Mt. Palgong, 12 Aug 2008, R.K. Duwal & S. Jung, 1 ♀ ( SNU); Geumhwa,-ri, Chilgok-gun, Gasan-myeon, 36.06611, 128.5575, 20 Aug 2012, H. Yoshitake, 2 ♀ ( NIAES). Gyeongsangnam-do: Geoje-si, Geoje Arboretum, 25–27 Aug 2008, R.K. Duwal and S. Jung, 2 ♂, 2 ♀ ( SNU). Jeollanam-do: Gwangyang-si, Choosan, 16–19 Jun 2008, R.K. Duwal & S. Jung, 2 ♂ ( SNU). NEPAL: Solukhumbu, Kenja – Ramechhap, Changma, 2,200m alt., 27.66, 86.45, 13 Oct 1979, M. Tomokuni, 1 ♂ ( NIAES); Kathmandu Valley, Lalitpur, Godawari, 27.577, 85.378, 27 Jun 2006, T. Yasunaga & R. K. Duwal, 1 ♂ ( NMTU).

Diagnosis. This is a closely related sibling species of P. typicus (Distant) , from which P. hyotan n. sp. can be distinguished by the characters mentioned in the above key, and different structures of the male and female genitalia, and presence of appressed, lanceolate setae on median part of scutellum.

Description. Body generally fuscous, antlike, small, rather strongly constricted at middle (HCR = 0.64–0.65 in average); dorsal surface weakly shining, with uniformly distributed, simple, brown or golden-brown setae. Head shiny fuscous, usually tinged with red below eyes, slightly wider than high. Antenna dark brown; basal part of segment I more or less whitish brown; segment II sometimes tinged with red, clavate; basal 1/3–1/2 of segment III and extreme base of IV creamy white. Labium shiny reddish brown, reaching apex of mesocoxa; segments III and IV creamy white; apical half of segment IV infuscate. Pronotum fuscous, shining, narrow; scutellum fuscous, weakly shining, with clustered scale-like setae at each corner, sparsely distributed, simple, semierect setae, and reclining, lanceolate setae mesally (cf. Fig. 15 E–F); pleura dark brown; mesepimeron with clustered scale-like setae; scent efferent system grayish brown, with somewhat produced peritreme ( Fig. 15C ). Hemelytron more or less with grayish-silver pruinosity (probably due to reticular surface microstructure, cf. Fig. E–F) on corium and clavus (cf. Fig. 3 A, C ); median band of scale-like setae weakly winding, somewhat W-shaped; anterior 1/3 of corium with narrowly clustered scale-like setae; cuneus shining, without scale-like seta; membrane dark smoky brown. Coxae creamy white, except for wholly darkened mesocoxa; legs dark brown; profemur pale brown; each tibia pale brown, more or less darkened basally; metafemur weakly curved; each tarsus yellowish brown, with darkened apex; pretarsal structure as in Fig. 15I ; parempodia rather long. Abdomen shiny fuscous; sternum III with a pair of circularly clustered scale-like setae ( Fig. 3D ). Male genitalia ( Figs 9 A–E, I–K, 15G, 16A–F): Left paramere sprayed-out, widened, with apex of sensory lobe elongate, rounded, spatula-shaped ( Figs 9I , 15G , 16B ); right paramere elongateovoid, with pointed hypophysis; median process of endosoma almost straight, weakly curved ( Fig. 16F ). Female genitalia ( Figs 10 A–B, 16M–O): Sclerotized ring narrowly folded laterally ( Fig. 10 A–B); vestibular sclerite with right-lateral thumb-like knob ( Fig. 10B ); interramal lobe densely with 4–5 rows of developed spinules along distal margin ( Fig. 16 M–O).

Measurements. See Table 1.

Etymology. From a Japanese name of general Pilophorus species, Hyotan-kasumikame [= Gourd-shaped mirids]; a noun in apposition.

Biology. Field investigation from Mieda, Nagasaki City ( Fig. 8B , site 4) in 2018–2020 suggested this new species has at least three generations per year. The adult and immature forms were found throughout the year, but they seem to prefer epigeic habitat in winter. Under cold climatic condition both adults and nymphs were observed to stay on or near the ground surface densely covered with weeds. Beating or sweep-netting collection methods did not yield any specimens so engine-vacuum-netting was required for field sampling during the winter season (cf. Yasunaga et al., 2019; Tamada et al., 2020).

Most investigation sites where P. hyotan was found are grasslands or shrubs dominated by Artemisia herbs or Pueraria vines. Quite a few specimens were also collected from inflorescences of various dicot angiosperms (see above material section). Predation on aphids, psyllids, leafhoppers and whiteflies was frequently observed ( Fig. 3 E– F). All developmental stages of P. hyotan n. sp. were successfully reared ( Fig. 4 A–H) on fermented milk beverage, dried bloodworms and dried brine-shrimp eggs (cf. Fukuda et al., 2020).

Discussion. The Japanese population, which had been identified solely as the widespread P. typicus , was supposed to include two species groups (Yasunaga, 1999), and subsequent molecular analysis of mitochondrial DNA by Ito et al. (2009, 2011) also recognized that the species conventionally identified as P. typicus in Japan consisted of two genotypes. The present new species represents ‘clade II’ sensu Ito et al. (2011). A preliminary molecular analysis by one of the authors (Nakatani, unpublished data) evidently supports the presence of at least two cryptic siblings, or P. typicus and P. hyotan ( Fig. 8A ). Although the two clades have different distribution ranges in temperate climate zones in Japan and Korea (cf. Ito et al. 2011), we found the individuals of both groups occur in southwestern Japan including some subtropical islands of the Ryukyus (cf. Fig. 8A ), and Nepal, Taiwan and Vietnam. The current molecular-based results are provisional, as P. hyotan has been confirmed to be distributed over broader regions from the Japan archipelago to SE Asia, west to the Himalayas. Each species can be distinguished by characters in the above key (couplet 21). Nonetheless, it is sometimes difficult to make a correct identification by external characters alone, due to intraspecific variation in size and condition of specimen (vestiture liable to be rubbed away while collecting or mounting). Exact identification of such ambiguous specimens may be only performed by dissecting the genitalia; but usually the male can be determined readily by observing shape of the left paramere (in left lateral view, cf. Fig. 15 N–O vs. G).

During recent field investigations in Nagasaki City by the first author and NWHS members ( Fig. 8B ), populations of the present new species were collected principally at grasslands or shrubs on the outskirts of the town, foothills or near broadleaf forests (i.e. ‘Satoyama’ zone, cf. Berglund, 2008), whereas P. typicus was taken from vegetables, ornamental plants or weeds at parks and small gardens in urbanized zones and residential quarters (whitish areas on Fig. 8B ). Current evidence suggests that the two sibling species may segregate respective habitat, or niches. However, the origin and speciation pattern of each species are still enigmatic, because of their widespread distributions.

Figures

FIGURE 1. Habitus images of Pilophorus spp. A. P. choii ♂. B. P. maeharai, holotype ♂. C. P. niger ♀. D–E. P. pullulus, holotype ♀ (Taiwan). F–G. P. pullulus ♂ (Amami-Oshima Is., Japan).

FIGURE 2. Habitus images of Pilophorus spp., live individuals. A. P. erraticus ♂. B. P. erraticus ♀. C–D. P. pseudoperplexus ♂. E. P. nakatanii, holotype ♂. F. P. lucidus ♀.

FIGURE 3. Habitus images of Pilophorus hyotan n. sp. (A–F) and P. typicus (G–I), live adult individuals. A. ♂. B. ♀. C. ♀, ventral view. D. ♀, ventral view. E. ♀, praying on an aphid. F. ♀, praying on a leafhopper nymph. G. ♂, from Kathmandu, Nepal. H. ♀, Surin, Thailand. I. ♀, Nagasaki, Japan, ventral view.

FIGURE 4. Life cycle and immature stages of Pilophorus hyotan n. sp. (A–H) and P. typicus (I–J), laboratory observations in Nagasaki, Japan. A. Mating pair (♂ left). B. Eggs (exposed opercula) oviposited into border part between stem and root of Artemisia sp. C. First instar nymph, just after hatching. D. Same, before molting to 2nd instar. E. Second instar nymphs. F. Third instar nymph. G. Fourth instar nymph with 5th (left). H. Fifth instar nymph with its exuvia. I. Fourth instar nymph. J. Fifth instar nymph (feeding on brine-shrimp eggs) [MTNR = metanotal ridge].

FIGURE 5. Habitus images of Pilophorus spp., live adult individuals. A–B. P. satoyamanus n. sp. ♂ (images courtesy of M. Takai). C–D. P. okamotoi ♂. E. P. setulosellus n. sp. ♀ (courtesy of M. Takai). F. P. setulosus ♀.

FIGURE 6. Habitus images of conifer-inhabiting Pilophorus spp. (A–C) and Pherolepis spp. (D–H), live adults and 5th instar nymph (G). A. Pilophorus miyamotoi ♂. B. P. validicornis ♀ (image courtesy of M. Nozawa). C. P. tagoi ♀ (courtesy of M. Nozawa). D. Pherolepis hizenicus n. sp., ♂. E. Same, lateral view. F. Same, ♀. G. Same, 5th instar nymph, ♂. H. Pherolepis fasciatus ♀.

FIGURE 7. Male hind wings (A–D) and dorsal thoracic structure of 5th instar nymphs (E–F) of Pilophorus hyotan n. sp. (A, C, E) and P. typicus (B, D, F). A–B. Compound microscopic images. C–F. Scanning electron micrographs. Abbreviations: AT, abdominal tergum; MTN, metanotum (scutellar area); MTNR, metanotal ridge; MTWP, metanotal (hind) wing pad; SES, abdominal scent efferent system.

FIGURE 8. A. Provisional result of molecular analysis for Pilophorus hyotan n. sp. and P. typicus (a-j in black and white circles showing sampling sites on cladogram). B. Distribution pattern of P. hyotan n. sp. and P. typicus in Nagasaki City area, SW Japan (numbers in square brackets corresponding to those mentioned in material examined section of respective species).

FIGURE 9. Male genitalia of Pilophorus spp. A–E, I–K. P. hyotan n. sp. (from Nagasaki, Japan: A–C, K; Solkhumbu, Nepal: D–E, I–J). F–H, L–N. P. typicus (Nakhon Nayok, Thailand: F–G; India: H, L–M; Nagasaki: N). O. P. miyamotoi (Kochi Pref., Japan). P–S. P. pullulus (Amami-Oshima Is.). A– B, D, F–G, O–P. Endosoma (vesica). C, E, H, S. Phallotheca. I–N, Q–R. Parameres.

FIGURE 10. Male genitalia of Pilophorus spp. A–B. P. hyotan n. sp. (from Tokyo, Japan). C–E. P. typicus (Nagasaki, Japan: C; India: D; Palawan, Philippines: E).

FIGURE 15. Scanning electron micrographs for Pilophorus hyotan n. sp. (with black circles●) and P. typicus. A. Left lateral habitus. B, K. Dorsal habitus. C, L. Thoracic pleura, left lateral view. D, J. Ventral habitus. E, F, M. Scutellum. G, N, O. Apex of pygophore (with sensory lobe of left paramere), left lateral view. H–I, P–Q. Metatarsus. G. Same, pretarsal structure.

FIGURE 16. Scanning electron micrographs of male (A–J) and female (K–O) genitalia for Pilophorus hyotan n. sp. (with black circles●) and P. typicus. A, H. Pygophore, dorsal view. B. Left paramere. C. Right paramere. D, G. Same, with exposed endosoma (vesica). E–F, I–J. Endosoma. K–O. Posterior wall of bursae.