Heteropterus Revista de Entomología 2020 Heteropterus Rev. Entomol. 20(1): 1-20 ISSN: 1579-0681

Two new species of the plant bug genus Melanotrichus inhabiting halophytes in southwestern Japan (Hemiptera: Heteroptera: Miridae)

T. YASUNAGA1, T. SHISHIDO2

1Research Associate; Division of Invertebrate Zoology; American Museum of Natural History; New York, NY 10024; USA; E-mail: [email protected] 2Katsuhara-ku; Shimo-oda 325-3; Himeji; Hyogo 671-1201; Japan; E-mail: [email protected]

Abstract The Japanese species of the orthotyline plant bug genus Melanotrichus Reuter, 1875 are reclassified. Two congeners uniquely inhabiting halophytes at a mixohaline river estuary in Hyogo Prefecture, M. fukudo n. sp. (associated with Artemisia fukudo of the Asteraceae) and M. halimus n. sp. (Suaeda maritima, Amaranthaceae), are described as new, with information on the biology and immature forms. A checklist of Melanotrichus species known from Japan and adjacent areas (Korean Peninsula and Taiwan) and a key to Japanese species are provided. The systematic position of the genus in the tribe Orthotylini is also discussed. Key words: Hemiptera, Heteroptera, Miridae, Melanotrichus, new species, Japan, halophytes.

Resumen Dos nuevas especies del género Melanotrichus habitantes de halófitos en el suroeste de Japón (Hemiptera: Heteroptera: Miridae) Se reclasifican las especies japonesas del género de míridos ortotilinos Melanotrichus Reuter, 1875. Se describen dos nuevas especies del género que habitan en halófitos de un estuario fluvial mixohalino en la Prefectura de Hyogo: M. fukudo n. sp. (asociada con Artemisia fukudo, Asteraceae) y M. halimus n. sp. (con Suaeda maritima, Amaran- thaceae). Se ofrece tanto la lista de las especies de Melanotrichus conocidas de Japón y áreas próximas (Península Coreana y Taiwán) como una clave para las especies de Japón. También se discute la posición sistemática del género dentro de la tribu Orthotylini. Palabras clave: Hemiptera, Heteroptera, Miridae, Melanotrichus, especies nuevas, Japón, halófitos.

Laburpena Melanotrichus generoko bi espezie berri Japoniaren hegomendebaldeko halofitoetakoak (Hemiptera: Heteroptera: Miridae) Mirido ortotilinoen Melanotrichus Reuter, 1875 generoaren Japoniako espezieak birsailkatzen dira. Bi espezie berri deskribatzen dira genero honetan, Hyogo Prefekturako ibai-estuario mixohalino baten halofitoak habitatzen dituztenak: M. fukudo n. sp. (Artemisia fukudorekin lotuta, Asteraceae) eta M. halimus n. sp. (Suaeda maritimarekin, Amaranthaceae). Japoniako zein hurbileko zonaldeetako (Korear Penintsula eta Taiwan) Melanotrichus generoaren espezie ezagunen zerrenda ematen da, bai eta Japoniako espezieetarako klabe bat ere. Halaber, genero honen Orthotylini tribuaren barruko kokapen sistematikoa eztabaidatzen da. Gako-hitzak: Hemiptera, Heteroptera, Miridae, Melanotrichus, espezie berriak, Japonia, halofitoak. 2 YASUNAGA, SHISHIDO: Two new species of Melanotrichus from Japan (Heteroptera: Miridae)

Introduction concentration (Kim et al., 2008). A halophilic flora dominated by vulnerable halophytes, Artemisia fukudo Melanotrichus Reuter, 1875 is one of the most speciose Makino (Asteraceae) (Fig. 1b) and Suaeda maritima (L.) genera within the plant bug subfamily Orthotylinae, Dumort (Amaranthaceae) (Fig. 1c), narrowly remains composed of more than 70 valid species spread over at the collecting site.Three additional species were the Holarctic, Oriental and Afrotropical regions collected and observed by the first author: M. choii (Schuh, 2002-2013; Yasunaga and Duwal, 2017; Au- (Josifov, 1976) and M. parvulus (Reuter, 1879) were kema, 2018). The majority of members are known to captured at west coast of Korea in Sep, 1998 (from be associated with Amaranthaceae herbs, and some Suaeda maritima, Salicornia europaea) (Fig. 1d), and species are restricted to halophilic goosefoots, such M. thaimaritimus at several sites (Bangkok, Chon Buri, as Salicornia, Salsola or Suaeda spp., grown at coastal Samut Prakan) along the Gulf of Siam, Thailand in zones (cf. Wagner, 1974; Liu and Zheng, 2014). 2010-2014 (Suaeda maritima) (cf. Fig. 1e; Yasunaga and However, these halophytes are presently endangered Duwal, 2017). or already extirpated in quite a few maritime areas in Approximately 450 dry-preserved specimens of six Japan, having been seriously degraded by reclamation, Asian congeners of Melanotrichus were examined. concrete seawalls, and/or pollution (cf. Shishido and The specimens examined in this study are deposited Yasunaga, 2016; Yasunaga et al., 2018). Therefore, the in the following collections: halophyte-inhabiting plant bugs are considered as AMNH: American Museum of Natural History, valuable bioindicators for assessing the quality of the New York, USA. littoral environment. CNC: Canadian National Collection, Ottawa, Based on hundreds of specimens collected from two Ontario, Canada. halophytes (Artemisia fukudo and Suaeda maritima, both designated officially as vulnerable species) by the NIAES: Division of Informatics and Inventory, second author at Motokawa River estuary, Hyogo, Institute of Agro-Environmental Sciences Japan, we provisionally reported two orthotyline spe- (NARO), Tsukuba, Ibaraki, Japan. cies, Melanotrichus choii (Josifov, 1976) and M. parvulus OMO: Otaru Museum, Otaru, Japan. (Reuter, 1879), as endangered mirid species (Shishido SCH: T. Shishido collection, Hyogo, Japan. and Yasunaga, 2016). However, our recent reassess- TYCN: T. Yasunaga collection, Nagasaki, Japan. ment of their morphological characters and host association confirmed that these doubtlessly represent Matrix code labels, which uniquely identify each two undescribed species. specimen and are referred to as «unique specimen In the present paper, two new species are described, identifier» (USI), are attached to the holotypes and namely M. fukudo n. sp. (inhabiting Artemisia fukudo) some representative specimens.The USI codes (e.g. and M. halimus n. sp. (Suaeda maritima). The immature AMNH_PBI 0012345) comprise an institution and forms are also documented briefly, with their con- project code (AMNH_PBI) and a unique number firmed host association and habitat preferences, for (0012345). These data were digitized on the Arthropod both species. A checklist of Melanotrichus species Easy Capture (formerly the Planetary Biodiversity known from Japan and adjacent areas as well as a key to Inventory) database maintained by the American Japanese species are provided. The systematic position Museum of Natural History, New York, USA of the genus in the tribe Orthotylini is also discussed. (http://research.amnh.org/pbi/) and are also search- able (by species name) on «Heteroptera Species Pages» (http://research.amnh.org/pbi/heteroptera- speciespage/). Material and methods Terminology mainly follows Yasunaga (1999) and Ya- sunaga and Duwal (2017) which treated Asian Melano- Field investigation to collect and observe two unde- trichus fauna; terminology for the genitalic structures scribed species was performed by the second author employed by Schwartz (2011) is also included. Only (mostly in Sep-Oct, 2014) at a Motokawa River estu- selected references are cited for known taxa, as more ary in Hyogo Prefecture (34º46’38’’N 134º34’08’’E), than a few comprehensive catalogs are now available facing the Seto Inland Sea (Setonaikai) which lies (Henry and Wheeler, 1988; Schuh, 1995; Kerzhner between the Japanese main islands of Honshu, Shi- and Josifov, 1999; Schuh, 2002-2013; Aukema et al., koku and Kyushu (Fig. 1a), with 28-34‰ salinity 2013; Aukema, 2018). Heteropterus Rev. Entomol. (2020) 20(1): 1-20 3

(a)

(f) (c) (b)

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FIGURE 1. Typical habitats and host plants of some Asian halophilic Melanotrichus spp.: (a) Habitat for two new species, M. fukudo n. sp. and M. halimus n. sp. at estuary of Motokawa River, Hyogo, Japan; (b) Community of Artemisia fukudo and Suaeda maritima (left) at water margin; (c) Suaeda maritima; (d) Vegetation of halophytes, Salicornia europaea L. and Suaeda maritima (L.) Dumort, at Gyonggi Bay, Korea (37.155, 126.690); (e) Suaeda maritima community at Bang Saen coast, Chon Buri, Thailand (13.3031, 100.9190; March 2010), which is now threatened by recent residential land development; (f) Example of reclamation that nearly exterminated halophytes in Isahaya City, Nagasaki Prefecture, SW Japan.

Scanning Electron Micrographs were taken with a All measurements are given in millimeters; for some Hitachi Tabletop Microscope® TM3030; the genitalic of the SEM images, scale bars are shown in micro- structures were also observed using a Nikon Eclipse meters (µm). Ci upright microscope, with a photophase unit. 4 YASUNAGA, SHISHIDO: Two new species of Melanotrichus from Japan (Heteroptera: Miridae)

Taxonomy vertex; small-sized male parameres; simple endosoma, cf. Fig. 5c; narrow interramal lobe, cf. Fig. 11a-i; and distinctly serrate ovipositor, cf. Figs. 6k, e, g, i, 11k-o). Genus Melanotrichus Reuter, 1875 In addition, halophyte specialists are unique to Mela- Melanotrichus Reuter, 1875: 151 (n. subgen. of Orthotylus notrichus members in the tribe Orthotylini; for in- Fieber, 1858), type species by subsequent designation stance, ten species are known to be associated with (Kirkaldy, 1906: 127): Phytocoris flavosparsus C.R. Sahlberg, Suaeda goosefoots (Henry, 1991; Schuh, 2002-2013). 1841; Schuh, 1995: 148 (cat.); Kerzhner and Josifov, 1999: The majority of Orthotylus (s. str.) species are arboreal, 255 (cat.); Yasunaga, 1999: 155 (diag.); Yasunaga et al., predominantly found on deciduous broadleaf trees, 2001: 139 (diag.); Schuh, 2002-2013 (online cat.); Liu and whereas Melanotrichus species preferably inhabit Ama- Zheng, 2014: 153 (diag.); Shishido and Yasunaga, 2016: ranthaceae or Asteraceae herbs, including halophilic 23 (diag.); Aukema, 2018 (online cat.). species. Based on the morphological and ecological Melanotrichus (as full genus): Knight, 1927: 142; Henry and evidences, Melanotrichus and Orthotylus are considered Wheeler, 1988: 427 (cat.); Henry, 1991: 449 (diag.); Yasu- to be not closely related to each other. Morpholo- naga and Duwal, 2017: 282 (taxonomic note). gically, Melanotrichus species have small-sized (some- times very tiny) parameres, simple endosoma (vesica), Diagnosis: and small interramal lobe, reminiscent of those Distinguished from other orthotyline genera by possessed by some taxa of Zanchius group rather than the following combination of characters: small size true Orthotylus and its allied genera. (2.2-4.5 mm in total length); generally pale green to Because of unique host association with vulnerable dull brown, or sometimes uniformly reddish colora- halophytes, some species of Melanotrichus are regarded tion (M. rubidus (Puton, 1874), cf. Wachmann et al., as bioindicators for assessing the quality of the 2004); dorsum with both simple and silvery scalelike coastal environment (cf. Shishido and Yasunaga, 2016). or flattened, lanceolate setae; small eyes contiguous Two new species described below were confirmed to to anterior margin of pronotum; anteriorly pointed inhabit Artemisia fukudo and Suaeda maritima, both of head with produced clypeus; basal carina on vertex; which are listed in the official Red Lists (cf. Kaneko wide scutellum that is wider than mesal length; rather and Nohara, 2014). Recent reclamation project for the thin, delicate hemelytron; small-sized male genital seg- Isahaya Bay, southwestern Japan (Fig. 1f) has almost ment and parameres; parameres more or less covered exterminated such halophyte community (e.g. Kawa- with micro-setae; C-shaped left paramere more or less kami et al., 2007), possibly along with quite a few curved inward; simple endosoma without serrate lobe; associated insect species. In some areas of Thailand, narrow interramal lobe; and distinctly serrate apex of Suaeda maritima communities are being also degraded gonapophysis II. rapidly by residential land development (Yasunaga, pers. obs., cf. Fig. 1e). Much broader survey on the Distribution: faunas restricted to such vulnerable or endangered Holarctic, Oriental and Afrotropical regions; in east- halophytes is urgently required for proper conser- ern Asia Melanotrichus members are currently known vation of maritime environment, as suggested by from China, Japan, Korea, Russian Far East, Taiwan Shishido and Yasunaga (2016). and Thailand. Poppius (1915) described Melanotrichus orientalis from southwestern coastal township in Taiwan (Anping, Discussion: Tainan City, 22º59’N 120º09’E). Judging from images Melanotrichus was erected as a subgenus of Orthotylus of the type specimens on website (http://twinsect Fieber, 1858 but was already regarded as a full genus type.nmns.edu.tw/specimen/?id=NMNS-HNHM- mainly by North American workers (e.g. Knight, 1927; 00068), this Taiwanese taxon is very similar to Henry and Wheeler, 1988; Henry, 1991). As argued M. parvulus, and the unequivocal identity of M. orien- by Yasunaga and Duwal (2017), Melanotrichus is well talis needs to be ascertained by examination of the defined as an independent genus by the unique char- genitalic structure. acters evidently different from those possessed by the Incidentally, Liu and Zheng (2014) recorded a Eu- nominotypical Orthotylus or other superficially similar ropean species, M. schoberiae (Reuter, 1876), from orthotyline genera (small size; both dark simple and China, with the plant association as Artemisia silvery flattened setae on dorsum; small eyes; wide selengense. However, M. schoberiae was reported Heteropterus Rev. Entomol. (2020) 20(1): 1-20 5

(a) (b)

(c) (d) (e)

(f) (g)

(j)

(h) (i)

FIGURE 2. Habitus images of Japanese Melanotrichus species, live individuals: (a)-(e) M. fukudo n. sp.; (f)-(j) M. halimus n. sp. / (a), (f) Adult male; (b), (g) Adult female; (c), (i) 3rd instar nymph; (d) 5th instar female; (e), (j) 5th instar male; (h) 2nd instar.

to be associated with Amaranthaceae halophyte, European element from China also requires further Suaeda sp.(cf. Schuh, 2002-2013). The record of this verification. 6 YASUNAGA, SHISHIDO: Two new species of Melanotrichus from Japan (Heteroptera: Miridae)

Checklist of Melanotrichus species from Japan to be introduced from the Old World, cf. Wheeler and neighboring areas (Korean Peninsula and and Henry, 1992). Taiwan): M. fukudo n. sp. - Japan (SW Honshu: Hyogo Pref.). M. choii (Josifov, 1976) (Figs. 3a-b, 4c, 5j, 6i-j, 9a-i, M. halimus n. sp. - Japan (SW Honshu: Hyogo Pref.). 11a-c, k) - China, Korea. M. orientalis (Poppius, 1915) - Taiwan (Tainan: M. flavosparsus (C.R. Sahlberg, 1841) (Figs. 3e, 4d, 5a-c, Anping). 6a-c, 9j-o, 11d-f, l) - Japan (Hokkaido, Honshu, M. parvulus (Reuter, 1879) (Figs. 3c-d, 4e, 5k-l, 6k-l, Shikoku, Kyushu), Holarctic Region, Neotropical 10a-i, 11g-i, o) - Japan (Tsushima Island), NW China, Region (New World populations are considered Korean Peninsula, Kazakhstan, Russia, Ukraine.

Key to Japanese species of Melanotrichus:

(1) Body generally vivid green (when alive or in fresh specimens); silvery flattened setae on dorsum partly clustered or arranged in patches (Figs. 3e, 9l) ...... M. flavosparsus - Body pale green or yellowish green; silvery setae on dorsum uniformly or sparsely distributed, not clustered ...... 2

(2) Labium short, reaching but not exceeding base of mesocoxa (Fig. 4c) ...... M. halimus n. sp. - Labium long, reaching middle or apex of metacoxa (Figs. 4a, 7c) ...... 3

(3) Head width across eyes more than 0.75 mm; silvery setae on dorsum rather sparsely distributed; micro- vestiture on head, scutellum, propleuron and forewing densely distributed (Fig. 7d-f); associated with Artemisia fukudo ...... M. fukudo n. sp. - Head width across eyes less than 0.74 mm; silvery setae on dorsum uniformly and rather densely distributed; micro-vestiture on head, scutellum, propleuron and forewing sparser (Fig. 10d-f); associated with Suaeda maritima ...... M. parvulus

Descriptions of new species E134.569052, Artemisia fukudo, 27 Sep 2014, T. Shishido (AMNH, CNC, NIAES, SCH). %% && Melanotrichus fukudo 32 + 13 : Same data, except for date 5 Oct 2014 n. sp. (AMNH, OMO, SCH, TYCN). (Figs. 1a-b, 2a-e, 4a, 5d-e, 6d-f, 7, 11m, 12a-f) 10 %% + 5 &&: Same data, except for date 17 Sep 2018 (SCH). Melanotrichus parvulus (nec Reuter, 1879): Shishido and Yasu- 2 %% + 1 &: Same data, except for date 23 Oct 2014 (TYCN). naga, 2016: 24 (diagnosis, habitus image of adults and immature forms, biology). Diagnosis: Type material: Recognized by its moderate size; yellowish or pale olive green basic coloration (but easily fading to HOLOTYPE: %,JAPAN: Honshu, Hyogo Pref., stramineous after death); sparsely distributed silvery Tatsuno City, Mitsu-cho,Kariya, Motokawa River flattened setae on dorsum; dense micro-vestiture on estuary, N34.777432, E134.569052, Artemisia fukudo, head, scutellum, propleuron and forewing (Fig. 7d-f); 5 Oct 2014, T. Shishido (AMNH) (AMNH_PBI long labium exceeding apex of mesocoxa; triangular 00380659). sensory lobe of left paramere (Fig. 5d); and rounded, PARATYPES: 79 %% + 34 &&: rather enlarged interramal lobe of posterior wall 35 %% + 15 &&: JAPAN: Honshu, Hyogo Pref., Tatsuno City, (Figs. 6f, 7n) covered with brush- or comb-like micro- Mitsu-cho, Kariya, Motokawa River estuary, N34.777432, processes (Fig. 7o). Heteropterus Rev. Entomol. (2020) 20(1): 1-20 7

(a)

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FIGURE 3. Habitus images of Asian Melanotrichus species, live individuals: (a)-(b) M. choii (Korea); (c)-(d) M. parvulus (Korea); (e) M. flavosparsus (Hokkaido, Japan); (f), (g) M. thaimaritimus (Thailand) / (a), (c), (e) Adult female; (b), (d), (g) 5th instar nymph; (f) Adult male.

Distinguished from its assumed closest congener, setae on dorsum (Figs. 2a, 7a vs. 3c, 10a); wider sen- M. parvulus by the characters mentioned in the key, sory lobe (Fig. 5d) and shorter hypophysis (Fig. 7l) in addition to the following characters: Sparser silvery of left paramere; rather thin, not bulbous right para- 8 YASUNAGA, SHISHIDO: Two new species of Melanotrichus from Japan (Heteroptera: Miridae)

Body Head Vertex Pronotal Max Antennal length Labial Legth hind leg length width width width width seg II seg III length femur tibia

M. fukudo n. sp. % (n = 5) Min 2.66 0.74 0.36 0.90 0.99 0.95 0.72 1.01 0.90 1.39 Max 3.24 0.77 0.43 1.03 1.22 1.08 0.89 1.08 1.08 1.58 Mean 3.01 0.75 0.38 0.98 1.14 1.01 0.80 1.04 1.01 1.48 M. fukudo n. sp. & (n = 5) Min 2.79 0.77 0.40 0.94 1.22 0.95 0.77 1.00 0.99 1.51 Max 3.36 0.81 0.45 1.10 1.44 1.05 0.81 1.20 1.20 1.62 Mean 3.10 0.79 0.42 1.05 1.35 1.02 0.78 1.10 1.08 1.57

M. halimus n. sp. % (n = 5) Min 2.45 0.56 0.29 0.69 0.81 0.72 0.54 0.45 0.72 0.99 Max 2.61 0.61 0.32 0.76 1.04 0.77 0.68 0.60 0.89 1.20 Mean 2.54 0.60 0.31 0.72 0.90 0.74 0.63 0.54 0.83 1.11 M. halimus n. sp. & (n = 4) Min 2.57 0.60 0.34 0.78 0.95 0.72 0.68 0.54 0.86 1.15 Max 2.74 0.61 0.36 0.83 1.08 0.77 0.81 0.65 0.97 1.22 Mean 2.64 0.61 0.35 0.81 1.04 0.76 0.76 0.60 0.91 1.20

M. choii % (n = 3) Min 3.09 0.65 0.33 0.90 1.07 1.04 0.84 0.69 1.05 1.50 Max 3.33 0.69 0.35 0.99 1.17 1.05 0.89 0.72 1.13 1.58 Mean 3.20 0.67 0.34 0.94 1.11 1.05 0.86 0.70 1.09 1.53 M. choii & (n = 2) Min 3.20 0.67 0.34 0.94 1.11 1.05 0.86 0.70 1.09 1.53 Max 3.31 0.71 0.44 0.99 1.31 1.19 0.95 0.81 1.17 1.59 Mean 3.26 0.69 0.40 0.97 1.22 1.13 0.91 0.77 1.13 1.56

M. flavosparsus % (n = 3) Min 2.88 0.72 0.32 0.90 1.08 0.99 0.81 0.90 1.08 1.62 Max 3.06 0.76 0.32 0.94 1.17 1.08 0.86 0.94 1.08 1.62 Mean 2.95 0.74 0.32 0.93 1.11 1.04 0.87 0.94 1.08 1.62 M. flavosparsus & (n = 3) Min 2.93 0.65 0.36 0.99 1.17 0.94 0.77 0.97 1.08 1.48 Max 3.24 0.74 0.38 1.03 1.19 0.99 0.81 1.04 1.08 1.53 Mean 3.08 0.70 0.37 1.02 1.21 0.97 0.80 1.01 1.08 1.50

M. parvulus % (n = 5) Min 2.35 0.62 0.30 0.80 0.93 0.81 0.63 0.90 0.90 1.22 Max 3.01 0.74 0.36 0.95 1.17 1.07 0.87 1.07 1.16 1.64 Mean 2.72 0.68 0.34 0.87 1.03 0.89 0.71 0.96 1.01 1.37 M. parvulus & (n = 4) Min 2.92 0.69 0.38 0.95 1.20 0.90 0.75 1.10 1.02 1.35 Max 3.01 0.74 0.42 0.99 1.34 1.05 0.78 1.13 1.08 1.62 Mean 2.97 0.72 0.40 0.97 1.25 0.97 0.77 1.11 1.05 1.52

TABLE 1. Measurements for Melanotrichus spp.

mere (Figs. 5d, 7k); flattened scales on interramal Description: lobe (Fig. 7o); broader ovipositor (gonapophysis II, Male: Macropterous. Body elongate-ovoid, compar- Fig. 6e); generally brownish or olive green immature atively large within congeners; basic coloration pale forms (Figs. 2c-e vs. 3d); and plant association with brownish green or olive (but often fading to stramin- Asteraceae host, Artemisia fukudo (Fig. 1b), instead of eous brown in dry-preserved specimens, cf. Fig. 4a); Amaranthaceae goosefoots (Fig. 1c-e). dorsal surface weakly shining (possibly due to dense Heteropterus Rev. Entomol. (2020) 20(1): 1-20 9

(c) (d) (a)

(b) (e)

FIGURE 4. Ventral habitus images of Asian Melanotrichus species, dry-preserved specimens: (a) M. fukudo n. sp.; (b) M. halimus n. sp.; (c) M. choii (Korea); (d) M. flavosparsus (Hokkaido, Japan); (e) M. parvulus (Korea).

micro-vestiture), with uniformly distributed, dark, basal width of pronotum. Labium pale brown, some- simple, semierect setae mixed with sparsely distrib- what tinged with red, reaching but not exceeding apex uted, silvery, flattened setae (Fig. 2a); dorsum (head, of mesocoxa; apical half of segment IV infuscate. scutellum, propleuron and hemelytron in particular) Pronotum weakly shining, partly speckled with yellow, densely covered with micro-vestiture as in Fig. 7d-g. with densely distributed micro-vestiture; scutellum and Head rather rounded, weakly produced anteriorly propleuron with densely distributed micro-vestiture; (Fig. 7b), with distinct basal carina on vertex (Figs. scent efferent system ivory white. Hemelytron some- 2a, 7a). Antenna uniformly pale grayish brown; seg- what matte, with densely distributed micro-vestiture; ment II about as long as labium, slightly longer than membrane pale smoky brown, with densely distributed 10 YASUNAGA, SHISHIDO: Two new species of Melanotrichus from Japan (Heteroptera: Miridae)

(b) (c)

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(d) (k) (j)

(e) (l)

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FIGURE 5. Male genitalia of Asian Melanotrichus species: (a)-(c) M. flavosparsus; (d)-(e) M. fukudo n. sp.; (f)-(i) M. halimus n. sp.; (j) M. choii; (k)-(l) M. parvulus / (a) Pygophore, in left-lateral view; (b), (d), (f), (j) Same, in ventral view; (g) Same, in caudal view; (c) Endosoma (vesica); (e), (h), (k) Left paramere; (i), (l) Right paramere. Heteropterus Rev. Entomol. (2020) 20(1): 1-20 11

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(j)

FIGURE 6. Female genitalia of Asian Melanotrichus species: (a)-(c) M. flavosparsus; (d)-(f) M. fukudo n. sp.; (g)-(h) M. halimus n. sp.; (i)-(j) M. choii; (k)-(l) M. parvulus / (a), (d) Bursa copulatrix, in dorsal view; (b), (e), (g), (i), (k) Ovipositor (gonapophysis II); (c), (f), (h) (j), (l) Posterior wall of bursae. 12 YASUNAGA, SHISHIDO: Two new species of Melanotrichus from Japan (Heteroptera: Miridae)

micro-vestiture elongate, with vein rather rounded Remarks: posteriorly. Legs pale green (stramineous brown in The breeding host of the mirid, Artemisia fukudo, is dried specimens); apical half of each tarsomere III liable to remain submerged in brine or mixohaline darkened; meta-tarsomere II about as long as III; water during high tides (cf. Ishikawa and Kachi, 2000; pretarsal structure as in Fig. 7i; parempodia ribbon- Kaneko and Nohara, 2014). Nonetheless, Melano- like, widened towards apex. Abdomen pale green trichus fukudo n. sp. was found to survive on the (stramineous brown in dried specimens) (Fig. 4a). halophyte, possibly due to possession of the micro- Male genitalia (Figs. 5d-e, 7j-l): Parameres gen- vestiture densely covering the body (e.g. Figs. 7d-f, erally wide, widely covered with minute setae; left 12c-e), which is reminiscent of the surface structure paramere subtriangular, not strongly curved (or of certain aquatic or semi-aquatic heteropterans.This curled), with laterally notched sensory lobe and unique character was observed both in adult (Fig. 7d-f) slender hypophysis (Fig. 7l); right paramere with rather and immature forms (Fig. 12c-e). The micro-vestiture flat sensory lobe and flat, blunt-tipped hypophysis is assumed to be equipped for adaptation to the (Fig. 7k); endosoma simple. unique host association at estuarine tidal flats. Female: As in male, but body oval, wider and slightly longer than male (Figs. 2b, 4a). Antennal segment II as long as or slightly shorter than basal width of pro- notum. Labium longer, reaching base of metacoxa. Melanotrichus halimus n. sp. Female genitalia (Figs. 6d-f, 7m-o, 11m): Bursa (Figs. 1a-c, 2f-j, 4b, 5f-i, 6g-h, 8, 11n, 12g-l) copulatrix with weak, thin-rimmed sclerotized ring (Fig. 6d); posterior wall with semi-circular interramal Melanotrichus choii (nec Josifov, 1975): Shishido and Yasu- lobe (Figs. 6f, 7m-n) that is densely covered with naga, 2016: 27 (diagnosis, habitus images of adults and comb-like, thin micro-processes (Fig. 7o); ovipositor immature forms, biology); Yasunaga et al., 2018: 93 (host, (gonapophysis II) sword-like, rather broad, sharply habitat). serrate along apical margin (Figs. 6e, 11m). Measurements: Type material: See Table 1. Holotype male: Total length of body 2.94; HOLOTYPE: %,JAPAN: Honshu, Hyogo Pref., head width across eyes 0.75; vertex width 0.36; lengths Tatsuno City, Mitsu-cho,Kariya, Motokawa River of antennal segments I-IV 0.26, 0.96, 0.77, 0.48; estuary, N34.777432, E134.569052, Suaeda maritima, length of labium 1.04; basal width of pronotum 0.96; 5 Oct 2014, T. Shishido (AMNH) (AMNH_PBI maximum width across hemelytron 1.14; and length 00380660). of metafemur 1.05 and tibia 1.50. PARATYPES: 80 %% + 42 &&: 11 %% + 11 &&:JAPAN: Honshu, Hyogo Pref., Tatsuno City, Etymology: Mitsu-cho,Kariya, Motokawa River estuary, N34.777432, From the specific name of Artemisia fukudo Makino, E134.569052, Suaeda maritima, 23 Sep 2014, T. Shishido (SCH). confirmed host plant of this new species («Fukudo» 15 %% + 9 &&: Same data, except for date 27 Sep 2014 (SCH). is also the Japanese name of this plant); a noun in 24 %% + 18 &&: Same data, except for date 5 Oct 2014 apposition. (AMNH, SCH, TYCN). 30 %% + 4 &&: Same data, except for date 17 Sep 2018 Distribution: (CNC, OMO, NIAES, SCH). Japan (SW Honshu: Hyogo Pref.). Diagnosis: Biology: Recognized primarily by its small size; clear pale green Both adults and immature forms were found from a basic coloration (but often fading to stramineous salt tolerant mugwort, Artemisia fukudo Makino after death); uniformly distributed dark simple setae (see below Remarks), in September and October. and silvery flattened setae on dorsum (Figs. 2f, 8a-d) Currently, the mirid is assumed to have a univoltine that is rather shiny and lacking dense micro-vestiture; life cycle and to overwinter in the egg stage. However, short labium only reaching base of mesocoxa; further field observation in spring and summer season strongly curved (curled) left paramere with both (May-August) is required to verify the whole annual tips of sensory lobe nearly contiguous to each other life cycle. (Figs. 5h, 8h); and ovoid interramal lobe of posterior Heteropterus Rev. Entomol. (2020) 20(1): 1-20 13

(a)(b) (c)

(d) (e) (f)

(g) (h) (i)

(k)

(j) (l)

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FIGURE 7. Scanning electron micrographs for M. fukudo n. sp. (M: male; F: female): (a) Head and pronotum in dorsal view; (b)-(c) Anterior body: (b) In lateral view; (c) In ventral view; (d)-(f) Microstructures of: (d) Head; (e) Pronotum, scutellum and clavus; (f) Propleuron; (g) Vestiture on corium; (h)-(i) Metatarsus; (j) Male genital segment in dorsal view; (k) Right paramere; (l) Left para- mere; (m) Female posterior wall; (n)-(o) Interramal lobe. 14 YASUNAGA, SHISHIDO: Two new species of Melanotrichus from Japan (Heteroptera: Miridae)

wall (Figs. 6h, 8j, k) densely covered with brush-like Female genitalia (Figs. 6g-h, 8j-l, 11n): Bursa copu- micro-processes (Fig. 8l). latrix with almost reduced sclerotized ring (Fig. 6h); Distinguished readily from its assumed sister species, posterior wall with ovoid interramal lobe (Figs. 6h, M. choii by the characters mentioned in the key, 8j-k) that is densely covered with brush-like (or partly and the following characters: Obviously smaller size hair-like) micro-processes (Fig. 8l); ovipositor (go- (cf. Fig. 4b vs. 4c, Table 1); pale green dorsum partly napophysis II) rather narrow, minutely and sharply tinged with yellow; shorter labium that is as long as serrate along apical margin (Figs. 6g, 11n). or less than head width across eyes; left paramere Measurements: with deeply serrate lateral edge of sensory lobe that See Table 1. Holotype male: Total length of body 2.57; densely bears stiff setae (Fig. 8h); wide and flattened head width across eyes 0.56; vertex width 0.30; lengths hypophysis of right paramere (Fig. 8i); and more of antennal segments I-IV 0.20, 0.75, 0.68, 0.39; strongly serrate apical margin of ovipositor (gona- length of labium 0.56; basal width of pronotum 0.69; pophysis II, Figs. 6g, 11n); and immature forms maximum width across hemelytron 1.04; and length more or less tinged with brown or yellow (Figs. 2h-j of metafemur 0.89 and tibia 1.20. vs. 3b). Etymology: Description: From Greek, halimon (halophilic goosefoots), referring Male: Macropterous. Body elongate-oval, parallel- to plant association of this new species; the specific sided, small; basic coloration clear pale green, partly name also sounds like «Harima» (= old name of a tinged with yellow (but easily fading to stramineous region including the type locality); an adjective to be brown in dry-preserved specimens as in Fig. 4b); treated as a noun in apposition. dorsal surface rather shining, lacking dense micro- vestiture, with uniformly distributed, dark, simple, Distribution: semierect setae and silvery, flattened setae. Head Japan (SW Honshu: Hyogo Pref.). (clypeus) rather produced anteriorly (Fig. 2f), with weak basal carina on vertex. Antenna uniformly pale Biology: brown; segment II about as long as or slightly longer than basal width of pronotum; segments III and IV The confirmed breeding host is a halophilic goose- brown to dark brown. Labium reddish brown, reaching foot, Suaeda maritima, on which both adult and imma- but not exceeding base of mesocoxa; apical 1/3 ture forms were found. Although the life cycle is of segment IV infuscate. Pronotum shining, rather probably similar to that of M. fukudo n. sp., further smooth; scent efferent system whitish brown. Heme- field investigation throughout a year is required to lytron shining, partly tinged with yellow; membrane verify their complete ecology. pale smoky brown, with vein somewhat angular pos- teriorly. Legs pale green (stramineous brown in dried specimens); apical half of each tarsomere III darkened; meta-tarsomere II slightly longer than III; pretarsal Acknowledgements structure as in Fig. 8f; parempodia ribbon-like, rather short. Abdomen pale green (stramineous brown in The first author is indebted to Prof.S.H. Lee (Division dried specimens) (Fig. 4b). of Entomology, Seoul National University,Korea) for Male genitalia (Figs. 5f-i, 8g-i): Parameres tiny organizing a trip to western coastal zone in Korea (less than 0.1 mm in length or width), partly covered (1999) to investigate heteropterans associated with with minute setae; left paramere C-shaped, strongly halophytes, to Ms.B.N.Rungrueang (Bangkok, Thai- curved (curled), with both tips of sensory lobe nearly land) for supporting field investigation in Thailand, contiguous to each other and lateral apex strongly and to Mr. D. Terada and Mr. A. Hama (CSR Di- setose (Figs. 5h, 8h); right paramere with flattened, vision, Hitachi High-Technologies Corporation, blunt-tipped hypophysis (Fig. 8i); endosoma simple. Tokyo) for generously allowing to use a tabletop Female: As in male, but body slightly wider and scanning electron microscope (demo unit). Thanks longer than male (Figs. 2g, 4b). Antennal segment II are extended to anonymous reviewers and editors for shorter than basal width of pronotum. Labium longer, improving the manuscript with useful comments and reaching apex of mesocoxa. suggestions. Heteropterus Rev. Entomol. (2020) 20(1): 1-20 15

(a)(b) (c)

(d) (e) (f)

(g) (h) (i)

(j) (k) (l)

FIGURE 8. Scanning electron micrographs for M. halimus n. sp. [(a)-(f) Females]: (a) Left lateral habitus; (b) Head; (c) Pronotum, scutellum and clavus; (d) Head and pronotum in left lateral view; (e)-(f) Metatarsus; (g) Male genital segment in dorsal view; (h) Left paramere; (i) Right paramere; (j) Female posterior wall; (k)-(l) Interramal lobe.

References the Heteroptera of the Palaearctic Region, vol. 6, supplement. The Netherlands Entomological Society. Amsterdam. AUKEMA B. 2018. Catalogue of the Palaearctic Heteroptera HENRY TJ. 1991. Melanotrichus whiteheadi, a new cruci- (searchable database). Available from: https://catpalhet. fer-feeding plant bug from the southeastern United linnaeus.naturalis.nl/. Last accessed: 7 Apr 2020. States with new records for the genus and a key to AUKEMA B, RIEGER CH,RABITSCH W. 2013. Catalogue of species of eastern North America (Heteroptera: Miri- 16 YASUNAGA, SHISHIDO: Two new species of Melanotrichus from Japan (Heteroptera: Miridae)

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FIGURE 9. Scanning electron micrographs for: (a)-(i) M. choii; (j)-(o) M. flavosparsus (M: male; F: female) / (a), (k) Anterior body in left lateral view; (b) Head; (c) Pronotum, scutellum and clavus; (d) Apices of labium, mandibular and maxillary stylets; (e) Thoracic pleurites; (f), (m), (n) Metatarsus; (g) Apex of pygophore, with left paramere and pygophoral processes; (h) Left and right para- meres; (i) Left paramere; (j) Head and pronotum in dorsal view; (l) Clustered scalelike setae on corium; (o) Male genital segment in left lateral view. Heteropterus Rev. Entomol. (2020) 20(1): 1-20 17

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FIGURE 10. Scanning electron micrographs for: (a)-(i) M. parvulus; (j)-(l) M. thaimaritimus (M: male; F: female) / (a), (j) Anterior body in dorsal view; (b) Thoracic pleurites; (c), (l) Metatarsus; (d)-(f) Microstructures of: (d) Head; (e) Pronotum, scutellum and clavus; (f) Propleuron; (g) Male genital segment in left lateral view; (h) Same, caudal view; (i) Apex of left paramere (hypophysis).

dae: Orthotylinae). Proceedings of the Entomological Society ISHIKAWA S, KACHI N. 2000. Differential salt toler- of Washington 93: 449-456. ance of two Artemisia species growing in contrasting HENRY TJ,WHEELER AGJR. 1988. Family Miridae coastal habitats. Ecological Research 15: 241-247. Hahn, 1833 (= Capsidae Burmeister, 1835). The plant JOSIFOV M. 1976. Drei neue Orthotylus-Arten aus bugs (pp.: 251-507). In: Henry TJ, Froeschner RC Korea. Reichenbachia 16: 143-146. (Eds.). Catalog of the Heteroptera, or true bugs of Canada KANEKO K, NOHARA S. 2014. The influence of and the continental United States. E.J. Brill. Leiden. changes in the degree and frequency of disturbance 18 YASUNAGA, SHISHIDO: Two new species of Melanotrichus from Japan (Heteroptera: Miridae)

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FIGURE 11. Scanning electron micrographs of female genitalia for: (a)-(c), (k) M. choii; (d)-(f), (l) M. flavosparsus; (g)-(i), (o) M. parvulus; (m) M. fukudo n. sp.; (n) M. halimus n. sp.; (j) M. thaimaritimus / (a), (d), (g) Posterior wall; (b), (c), (e), (f), (h), (i), (j) Interramal lobe; (k)-(o) Apex of ovipositor (gonapophysis II). Heteropterus Rev. Entomol. (2020) 20(1): 1-20 19

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FIGURE 12. Scanning electron micrographs for final (5th) instar nymphs of: (a)-(f) M. fukudo n. sp.; (g)-(l) M. halimus n. sp. / (a), (g) Dorsal habitus; (b), (h) Head in ventral view; (c), (i) Pronotum; (d), (j) Mesonotum; (e), (k) Mesonotal (right) and metanotal (left) wing-pads; (f), (l) Abdominal terga II-IV.

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