Abstract
Background
The predatory stink bug genus Picromerus Amyot & Serville, 1843 (Hemiptera, Heteroptera, Pentatomidae, Asopinae) comprises 11 species found in the Northern Hemisphere. In Japan, two species have been recorded to date. However, an easy-to-understand identification method, such as an illustrated key, is lacking. Currently, Picromerusgriseus (Dallas, 1851) has been recorded in Bangladesh, Bhutan, China, Indonesia, Myanmar, Pakistan and Taiwan, but not in Japan.
New information
Picromerusgriseus was recorded in Japan for the first time, based on a single individual collected from grasslands around the fields of Ishigaki Island of the Ryukyu Islands, which belong to the Oriental Region. This discovery represents the easternmost record of the species. An illustrated key to the species of Picromerus occurring in Japan is also provided.
Keywords: Heteroptera, Pentatomidae, Asopinae, Picromerusgriseus , stink bug, new record, illustrated key, Japan, Ryukyu Islands, Ishigaki Island, Oriental Region
Introduction
The stink bug subfamily Asopinae Spinola, 1850 comprises 303 species in 63 genera worldwide and all species for which their biology is known are predacious (Schuh and Weirauch 2020). The following twelve species in eight genera are known in Japan: Andrallusspinidens (Fabricius, 1787); Armacustos (Fabricius, 1794); Dinorhynchusdybowski Jakovlev, 1876; Eocantheconafurcellata (Wolff, 1811); E.japonica (Esaki & Ishihara, 1950); E.kyushuensis (Esaki & Ishihara, 1950); E.shikokuensis (Esaki & Ishihara, 1950); Picromerusbidens (Linnaeus, 1758); P.lewisi Scott, 1874; Pinthaeussanguinipes (Fabricius, 1781); Rhacognathuscorniger Hsiao & Cheng, 1977; and Zicronacaerulea (Linnaeus, 1758) (Ishikawa 2016). Two Japanese species, A.spinidens and E.furcellata, are expected to have some success in effectively utilising indigenous natural enemies through conservation (Rural Culture Association 2016).
The genus Picromerus Amyot & Serville, 1843 (Asopinae) comprises 11 species from the Northern Hemisphere: P.bidens; P.brachypterus Ahmad & Önder, 1990; P.conformis Herrich-Schäffer, 1841; P.elevatus Zhao, Liu & Bu, 2013; P.fasciaticeps Zheng & Liu, 1987; P.griseus (Dallas, 1851); P.lewisi; P.nigridens (Fabricius, 1803); P.orientalis Rishi & Abbasi, 1973; P.pseudobidens Ahmad & Önder, 1990; and P.viridipunctatus Yang, 1934 (Thomas 1994, Rider 2006, Zhao et al. 2013). In Japan, two species, P.bidens and P.lewisi, were only recorded from Japan proper and its surrounding islands, which belong to the Palearctic Region (Ishikawa 2016), while no species have been recorded from the Ryukyu Islands, whose central and southern parts belong to the Oriental Region. These two species are so similar that it is difficult to distinguish them at first glance. Although some field guides and pictorial books dealing with Japanese Asopinae have been published (e.g. Yasunaga et al. (1993), Takai and Ishikawa (2012)), no identification key illustrating the diagnostic characteristics of the two species, based on the Japanese populations, has been provided for easier and more accurate identification. Therefore, field surveys on the Ryukyu Islands and publication of an illustrated key for Japanese Picromerus are needed to elucidate Asopinae in Japan and make this genus known to the public.
In autumn, 2022, the second author collected a single individual of an indeterminate species of Picromerus from the grasslands around the fields of Ishigaki Island of the Ryukyu Islands (Oriental Region). After the first author examined its morphological characteristics, we concluded that it belonged to P.griseus, which is currently known to occur in Bangladesh, Bhutan, China, Indonesia, Myanmar, Pakistan and Taiwan (Thomas 1994, Rider 2006, Zhao et al. 2013, Zheng and Lin 2013). Herein, we report P.griseus in Japan for the first time, representing the easternmost occurrence of this species. In addition, we provide an illustrated key for all three Japanese species of Picromerus.
Materials and methods
Morphological characteristics of dried specimens were observed using a stereoscopic microscope (SZ60; Olympus, Tokyo, Japan). To examine the genital characteristics, the male terminalia were removed from the body after softening the specimens in hot water. The removed genital capsule was immersed in hot 15% potassium hydroxide (KOH) solution for 5 min. For further observations, parameres were removed from the genital capsule soaked in 99% ethanol. Male genitalia were preserved in small polyethylene vials containing a 50% glycerine and 50% water solution. A polyethylene vial was mounted on the pin with the specimens. The specimens were photographed using a digital microscope (Dino-Lite Premier M; Opto Science, Tokyo, Japan) and a compact digital camera (Tough TG-6; Olympus) and image stacks were processed using Adobe Photoshop 2021 ver. 22.5.1 (Adobe Inc., CA, USA) when using the digital microscope. Measurements were obtained using a stereoscopic microscope equipped with an ocular grid and a digital microscope. Morphological terms were assigned as described by Tsai et al. (2011).
The single specimen of Picromerusgriseus examined in the present study was deposited at the Laboratory of Entomology, Faculty of Agriculture, Tokyo University of Agriculture, Kanagawa, Japan (TUA). Specimens of the Japanese species of Picromerus that were used for creating the identification key and for comparison with P.griseus were deposited in the Entomological Laboratory, Faculty of Agriculture, Kyushu University, Fukuoka, Japan (ELKU) and TUA.
Taxon treatments
Picromerus griseus
(Dallas, 1851)
77EEBAC0-304E-5F94-8CDF-CE8E4A7B3777
Cantheconagrisea Dallas, 1851 - Dallas (1851): 92, new species and description.
Picromerusobtusus Walker, 1867 - Walker (1867): 133, new species and description; Schouteden (1907): 25, synonymised with Picromerusgriseus.
Picromerusnigrivitta Walker, 1867 - Walker (1867): 133, new species and description; Distant (1900): 58, synonymised with Picromerusobtusus.
Picromerussundanus Breddin, 1902 - Breddin (1902): 96, new species and description; Thomas (1994): 192, synonymised with Picromerusgriseus. Gaedike (1971): 100, designation of lectotype.
Picromerusgriseus Schouteden, 1907 - Schouteden (1907): 25, new combination; Thomas (1994): 192, catalogue and distribution; Rider (2006): 243, catalogue and distribution; Zhao et al. (2013): 73, diagnosis, figure, and distribution; Zheng and Lin (2013): 145, figure and distribution.
Materials
Type status: Other material. Occurrence: recordedBy: Akihiro Utagawa; individualCount: 1; sex: male; lifeStage: adult; occurrenceID: B9C40A18-594B-59E7-BCA1-4AB46599AC3E; Taxon: scientificName: Picromerusgriseus (Dallas, 1851); namePublishedIn: 1851; kingdom: Animalia; phylum: Arthropoda; class: Insecta; order: Hemiptera; family: Pentatomidae; genus: Picromerus; specificEpithet: griseus; scientificNameAuthorship: Dallas; Location: islandGroup: Ryukyu Islands; island: Ishigaki Island; country: Japan; countryCode: Okinawa; municipality: Ishigaki-shi; locality: Sakieda; decimalLatitude: 24.438250; decimalLongitude: 124.102167; geodeticDatum: WGS84; Identification: identifiedBy: Jun Souma; dateIdentified: 2023; Event: samplingProtocol: none specified; eventDate: 08-11-2022; Record Level: institutionCode: TUA; basisOfRecord: PreservedSpecimen
Diagnosis
Picromerusgriseus can be distinguished from other species of the genus using a combination of the following characteristics: head, pronotum, scutellum and femora uniformly brown (Fig. 1a, b); humeral angle of pronotum strongly protruding laterad, acute at apex, posteriorly with a distinct subapical prominence (Fig. 2a); posterior margin of genital capsule weakly curved inwards in middle part (Fig. 4a); and paramere weakly curved inwards in apical part in dorsal and caudal views, distinctly concave along inner margin in dorsolateral view (Figs 3a, 5a, 6a).
Habitus of three species of Picromerus from Japan.
Figure 1a.
Picromerusgriseus, dorsal view.
Figure 1b.
Picromerusgriseus, ventral view.
Figure 1c.
Picromerusbidens, dorsal view.
Figure 1d.
Picromeruslewisi, dorsal view.
Heads and pronota of three species of Picromerus from Japan, dorsal view.
Figure 2a.
Picromerusgriseus.
Figure 2b.
Picromerusbidens.
Figure 2c.
Picromeruslewisi.
Genital capsules of three species of Picromerus from Japan, ventral view.
Figure 4a.
Picromerusgriseus.
Figure 4b.
Picromerusbidens.
Figure 4c.
Picromeruslewisi.
Genital capsules of three species of Picromerus from Japan, dorsal view.
Figure 3a.
Picromerusgriseus.
Figure 3b.
Picromerusbidens.
Figure 3c.
Picromeruslewisi.
Genital capsules of three species of Picromerus from Japan, caudal view.
Figure 5a.
Picromerusgriseus.
Figure 5b.
Picromerusbidens.
Figure 5c.
Picromeruslewisi.
Parameres of three species of Picromerus from Japan, dorsolateral view.
Figure 6a.
Picromerusgriseus.
Figure 6b.
Picromerusbidens.
Figure 6c.
Picromeruslewisi.
Distribution
Japan (Ryukyu Islands: Ishigaki Island), Bangladesh, Bhutan, China, Indonesia, Myanmar, Pakistan, Taiwan (Thomas 1994, Rider 2006, Zhao et al. 2013, Zheng and Lin 2013, present study).
The discovery of Picromerusgriseus from Japan represents the easternmost record of the species.
Biology
Picromerusgriseus was collected from grasslands surrounding fields in Japan. In Japan, adults are collected in November; however, the nymphs are unknown.
Taxon discussion
The specimen recorded above (Figs 1a, b, 2a, 3a, 4a, 5a, 6a) matched the photographs and descriptions (Dallas 1851, Zhao et al. 2013) of Picromerusgriseus in terms of morphological characteristics, including the humeral angle and male genitalia. The Japanese specimen was identified as P.griseus using a key for the East Asian species of Picromerus (Zhao et al. 2013), based on its morphological characteristics. However, the colouration of the connexivum of the Japanese specimen (yellow and black) did not match the above-mentioned key (entirely black). To the best of our knowledge, Japanese populations of P.bidens and P.lewisi show a high degree of intraspecific variation in the colouration of the connexivum (yellow and black to entirely black) (Figs 1c, d, 7). In conclusion, we did not use the colouration of the connexivum as a diagnostic characteristic of Picromerus and identified the Japanese specimen as P.griseus, based on the shape of the humeral angle and male genitalia.
Living individuals of two species of Picromerus from Japan.
Figure 7a.
Picromerusbidens.
Figure 7b.
Picromeruslewisi.
Checklists
Checklist of the species of Picromerus occurring in Japan
Picromerus bidens
(Linnaeus, 1758)
446F3361-8AD0-525D-9221-AEDDD875210B
Distribution
Afghanistan, Albania, Algeria, Armenia, Austria, Azerbaijan, Belgium, Bosnia Herzegovina, Bulgaria, Byelorussia, Canada, China, Croatia, Czech Republic, Denmark, Estonia, Finland, France, Georgia, Germany, Greece, Hungary, Iran, Ireland, Italy, Japan (Kunashiri Island, Hokkaido, Rishiri Island, Honshu), Kazakhstan, Kirgizia, Korea, Latvia, Liechtenstein, Lithuania, Luxemburg, Macedonia, Moldavia, Mongolia, Montenegro, Netherlands, Norway, Poland, Portugal, Romania, Russia, Serbia, Slovakia, Slovenia, Spain, Sweden, Switzerland, Tajikistan, Turkey, Ukraine, United Kingdom, USA, Uzbekistan (Thomas 1994, Kanyukova and Marusik 2006, Rider 2006, Takai and Ishikawa 2012, Aukema et al. 2013, Zhao et al. 2013, Ishikawa 2016, Roca-Cusachs et al. 2020).
Picromerus griseus
(Dallas, 1851)
193F1E3C-A7F4-5123-9FA6-6231EDC725B0
http://en.wikipedia.org/wiki/Atypus_affinis
Distribution
Bangladesh, Bhutan, China, Indonesia, Japan (Ishigaki Island), Myanmar, Pakistan, Taiwan (Thomas 1994, Rider 2006, Zhao et al. 2013, Zheng and Lin 2013, present study).
Picromerus lewisi
Scott, 1874
2C14B9D6-627C-5C5A-9583-5EBFCA81B192
Distribution
China, Japan (Hokkaido, Honshu, Sado Island, Awa Island, Shikoku, Kyushu, Tsushima Island, Shimokoshiki Island, Shimoshima Island), Kazakhstan, Korea, Russia, Taiwan (Yasunaga et al. 1993, Thomas 1994, Rider 2006, Takai and Ishikawa 2012, Aukema et al. 2013, Zhao et al. 2013, Zheng and Lin 2013, Ishikawa 2016, Nozaki et al. 2016, Roca-Cusachs et al. 2020).
Identification Keys
Key to the species of Picromerus occurring in Japan
| 1 | Humeral angle of pronotum posteriorly with a distinct subapical prominence (Figs 1a, 2a, b); lateral sides of abdomen without black spots on ventral surface; known from Ryukyu Islands | Picromerusgriseus (Dallas, 1851) |
| – | Humeral angle of pronotum without distinct subapical prominence (Figs 1c, d, 2b, c); lateral sides of abdomen with black spots on ventral surface; known from Japan proper and its surrounding islands | 2 |
| 2 | Humeral angle of pronotum strongly protruding laterad, acute at apex (Fig. 2b); posterior margin of genital capsule weakly curved inwards in middle part (Fig. 4b); paramere weakly curved inwards in apical part in dorsal and caudal views, distinctly concave in inner margin in dorsolateral view (Figs 3b, 5b, 6b) | Picromerusbidens (Linnaeus, 1758) |
| – | Humeral angle of pronotum weakly protruding laterad, obtuse at apex (Fig. 2c); posterior margin of genital capsule strongly curved inwards in middle part (Fig. 4c); paramere strongly curved inwards in apical part in dorsal and caudal views, slightly concave in inner margin in dorsolateral view (Figs 3c, 5c, 6c) | Picromeruslewisi Scott, 1874 |
The key below is based on morphological characteristics and colouration that are stable in the Japanese populations and the distribution of three species in Japan.
Supplementary Material
Acknowledgements
We express our sincere thanks to Nikolay Simov (National Museum of Natural History, Sofia, Bulgaria) and Marcos Roca-Cusachs (University of New South Wales, Sydney, Australia) for their critical comments on the manuscript. We would like to thank Toshiya Hirowatari, Satoshi Kamitani and Toshiharu Mita (ELKU) for allowing us to examine the specimens when the first author was a PhD student. This study was supported in part by a Grant-in-Aid for JSPS Fellows (JP20J20483) awarded to the first author from the Japan Society for the Promotion of Science, Tokyo, Japan. We would like to thank Editage (www.editage.jp) for English language editing.
References
- Aukema B., Rieger C., Rabitsch W. Catalogue of the Heteroptera of the Palaearctic Region. Vol. 6, Supplement. The Netherlands Entomological Society; Amsterdam, Netherlands: 2013. 629. [Google Scholar]
- Breddin G. Beiträge zur Kenntniss der malayischen und indischen Pentatomiden. Wiener Entomologische Zeitung. 1902;21:94–101. [Google Scholar]
- Dallas W. S. List of the specimens of hemipterous insects in the collection of the British Museum. Part 1. Trustees of the British Museum; London, United Kingdom: 1851. 368 [Google Scholar]
- Distant W. L. Rhynchotal notes.—V. Heteroptera: Asopinæ and Tessaratominæ. Annals and Magazine of Natural History (Series 7) 1900;6:55–64. doi: 10.1080/00222930008678340. [DOI] [Google Scholar]
- Gaedike H. Katalog der in den Sammlungen des ehemaligen Deutschen Entomologischen Institutes aufbewahrten Typen.—V. Beiträge zur Entomologie. 1971;21:79–159. [Google Scholar]
- Ishikawa T. In: Catalogue of the insects of Japan Volume 4 Paraneoptera. Hayashi M., Tomokuni T., Yoshizawa K., Ishikawa T., editors. Touka-shobo; Fukuoka, Japan: 2016. Family Pentatomidae.494–504. [Google Scholar]
- Kanyukova E. V., Marusik Y. M. A check-list of Heteroptera of the Kuril Islands and brief zoogeographical survey of the fauna. Biodiversity and Biogeography of the Kuril Islands and Sakhalin. 2006;2:161–174. [Google Scholar]
- Nozaki T., Nozaki Y., Uki K., Tsukada T. The heteropteran fauna in the Ushibuka area of the Amakusa Islands, Kumamoto Prefecture, Japan. Rostria. 2016;60:67–96. Japanese. [Google Scholar]
- Rider D. A. In: Catalogue of the Heteroptera of the Palaearctic Region. Vol. 5. Pentatomomorpha II. Aukema B., Rieger C., editors. The Netherlands Entomological Society; Amsterdam, Netherlands: 2006. Family Pentatomidae Leach, 1815.233–402. [Google Scholar]
- Roca-Cusachs M., Kim J., Park J., Jung S. Taxonomic review of the predatory stink bugs of the Korean Peninsula (Heteroptera: Pentatomidae: Asopinae), with a key to the Korean species and a discussion of their usefulness as biological control agents. Journal of Asia-Pacific Entomology. 2020;23:113–123. doi: 10.1016/j.aspen.2019.09.006. [DOI] [Google Scholar]
- Rural Culture Association, editor. 天敵活用大辞典. Rural Culture Association; Tokyo, Japan: 2016. 824. Japanese. [Google Scholar]
- Schouteden H. In: Genera Insectorum. Wytsman M. P., editor. Wytsman; Bruxelles, Belgium: 1907. Heteroptera, Fam. Pentatomidae, Subfamily Asopinae (Amyotinae)1–82 [Google Scholar]
- Schuh R. T., Weirauch C. True Bugs of the World (Hemiptera: Heteroptera). Classification and natural history (Second Edition) Siri Scientific Press; Manchester, United Kingdom: 2020. 768. [Google Scholar]
- Takai M., Ishikawa T. In: A field guide to Japanese bugs. Terrestrial heteropterans III. Ishikawa T., Takai M., Yasunaga T., editors. Zenkoku Noson Kyoiku Kyokai Publishing Co., Ltd.; Tokyo: 2012. Family Pentatomidae Leach, 1815 Stink bugs.466–497. Japanese. [Google Scholar]
- Thomas D. B. Taxonomic synopsis of the Old World Asopinae genera (Heteroptera: Pentatomidae) Insecta Mundi. 1994;8:145–212. [Google Scholar]
- Tsai J. F., Rédei D., Yeh G. F., Yang M. M. ewel bugs of Taiwan (Heteroptera: Scutelleridae) National Chung Hsing University; Taichung, Taiwan: 2011. 309. [Google Scholar]
- Walker F. Catalogue of the specimens of heteropterous Hemiptera in the collection of the British Museum. Part I. British Museum (Natural History); London, United Kingdom: 1867. 240 [Google Scholar]
- Yasunaga T., Takai M., Yamashita I., Kawamura M., Kawasawa T. A field guide to Japanese bugs. Terrestrial heteropterans. Zenkoku Noson Kyoiku Kyokai, Publishing Co., Ltd.; Tokyo, Japan: 1993. 380. Japanese. [Google Scholar]
- Zhao Q., Liu G., Bu W. A review of the Chinese species of the genus Picromerus Amyot and Serville, with description of a new species (Hemiptera: Heteroptera: Pentatomidae: Asopinae) Zootaxa. 2013;3613:146–164. doi: 10.5281/zenodo.5280138. [DOI] [PubMed] [Google Scholar]
- Zheng S., Lin Y. 椿象圖鑑. Morning Star Publishing Co., Ltd.; Taichung, Taiwan: 2013. 381. Chinese. [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.