Heteroptera: Miridae) from Thailand, with Descriptions of New Species and Immature Forms

First record of the plant bug subfamily Psallopinae (Heteroptera: Miridae) from Thailand, with descriptions of new species and immature forms

Tomohide Yasunaga, Kazutaka Yamada & Taksin Artchawakom

The plant bug subfamily Psallopinae Schuh is reported from Thailand, or continental Southeast Asia, for the first time. Two new species of the genus Psallops Usinger, 1946, P. fulvioides and P. sakaerat, are described from northeastern Thailand. The detailed habit and immature forms are described for P. fulvioides. The discovery also represents the first record of the immature stages for the subfamily. Habitus images of these new species are provided. Tomohide Yasunaga, JICA-SV, Rajamangala University of Technology Suvarnabhumi, Huntra Campus, 60 Moo 3 Asia R’d, Huntra, Phranakhon- Si-Ayutthaya 13000, Thailand; Research Associate, American Museum of Natural History, New York 10024. [email protected] Kazutaka Yamada*, Tokushima Prefectural Museum, Bunka-no-Mori Park, Mukôterayama, Hachiman-chô, Tokushima, 770-8070 Japan. [email protected] Artchawakhom Taksin, Director, Sakaerat Environmental Research Station, Thailand Institute of Scientific and Technological Research (TISTR), Ministry of Science & Technology, Wang Nam Khieo, Nakhon Ratchasima, 30370 Thailand. [email protected]

Introduction Almost nothing is known about the biology of this The Psallopinae form the smallest plant bug sub- small subfamily as most specimens have been collected family within the largest heteropteran family Miri- at light; thus habits and habitats of psallopines remain dae. Only eight extant species in two genera are unknown (Wheeler 2001). Only two Japanese species currently known (seven species in Psallops Usinger, have been collected by sweeping leaves or branches of 1946, from Japan, Saudi Arabia, and South Pacific broad-leaved trees (Yasunaga 1999, 2001). Islands, and Isometocoris blantoni Carvalho & Sailer, During our continuing fieldwork in Sakaerat 1954, from Panama), in addition to a Baltic amber National Environmental Research Station, north- fossil, Isometopsallops schuhi Herczek & Popov, 1992 eastern Thailand between July 2008 and June 2009, (Schuh 1995, Yasunaga 1999, 2001). eight adult specimens and two immature forms, rep- This little known subfamily was established by resenting two undescribed species of Psallops, have Schuh (1976) for a single member Psallops ocullatus been collected. Herein, we record the subfamily Psal- Usinger, 1946 that had been placed in the Phylinae lopinae from continental Southeast Asia for the first since the original description. Schuh (1976) sug- time, and describe Psallops fulvioides and P. sakaerat as gested that Psallops is defined amongst others by the new to science. The fourth and final instar nymphs of finely upturned anterior margin of the pronotum, P. fulvioides are documented, with information on one or two cells on the membrane, two-segmented the habitat. The discovery also represents the first tarsi, a subapical tooth of the claw, simple form of record of the immature stages of the Psallopinae. the vesica, and phallotheca fused with the phallobase. A checklist of the genus Psallops is provided.

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1 2

6 8 9

Figs 1–9. Psallops species in Thailand. – 1-3, P. sakaerat, males; 4-5, P. fulvioides, holotype female; 6, P. fulvioides, 4th instar nymph; 7-8, ditto, final instar nymph; 9, A fabaceous broadleaf, habitat of P. fulvioides.

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10 11

12 13 14

15 16 17

Figs 10–17. Habitus images of Psallops sakaerat (10) and P. fulvioides (11-17). – 10, ventral view of adult male; 11, ventral view of holotype female; 12-14, Dorsal (12), ventral (13) and left lateral (14) of final instar nymph; 15-17, Dorsal (15), ventral (16) and left lateral (17) of 4th instar nymph.

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Material and methods Discussion Dried specimens were used in general, but delicate As pointed out by Schuh (1976), Psallops evidently immature forms are preserved in 80% alcohol in contains quite a few undescribed species particularly a small vial. All type specimens designated in this in the Old World subtropics and tropics. Because study will be deposited in the Department of Ento- it is difficult to collect psallopines by sweeping or mology, American Museum of Natural History, New beating, their biology and immature stages were pre- York (AMNH) and T. Yasunaga Collection, Naga- viously unknown. Two Japanese species have occa- saki, Japan (TYCN). All measurements are given in sionally been collected from branches of broadleaved millimeters. In the synonymic list, only selected ref- trees (Yasunaga 1999, 2001). During our recent erences are cited as comprehensive catalogs are avail- fieldwork in Thailand, an adult and two immature able (Kerzhner & Josivov 1999, Schuh 1995). Dig- forms of an undescribed species (P. fulvioides), were ital images of live individuals were taken with Canon discovered as mentioned below. EOS Kiss Digital camera body + Canon-Olympus mount adapter + Olympus Macrophoto System Checklist (Auto Extension Tube with 35 mm macrolens and Psallops Usinger, 1946 T10 Ringflash). P. fulvioides Yasunaga & Yamada, sp. n. P. grandoculus Linnavuori & Alamy, 1982 P. myiocephalus Yasunaga, 1999 Taxonomy P. nakatanii Yasunaga, 1999 Psallops Usinger P. oculatus Usinger, 1946 P. ponapensis Carvalho, 1956 Psallops Usinger, 1946: 86 (gen. n. in subfam. Phylinae), P. sakaerat Yasunaga & Yamada, sp. n. type species: P. ocullatus Usinger, 1946; Schuh 1995: P. yaeyamanus Yasunaga, 1999 42 (cat.); Kerzhner & Josifov 1999: 7 (cat.); Yasunaga P. yapensis Carvalho, 1956 1999: 737 (diag., key to Japanese spp.); Yasunaga 2001: 122 (diag.). Psallops sakaerat Yasunaga & Yamada, sp. n. Diagnosis Figs 1–3, 10, 18, 20, 22–27 Recognized by the following diagnostic characters: Type material. Holotype ?, Thailand: Nakhon body small, 2–3.5 mm, ovoid to elongate oval; basic Ratchasima Prov., Wang Nam Khieo Dist., Sakaerat coloration brownish to fuscous; dorsal surface shin- Environmental Research Station, N14°30’26.9”, ing, partly roughened or shagreened, with uniformly E101°55’39.2” , 407m alt., light trap, 13.vi.2009, distributed, dark, simple, semierect setae; head short; T. Yasunaga & K. Yamada. Paratypes: 1?, same eyes enlarged especially in ?, occupying most part data as for holotype; 2?, same data except for date: of head; vertex very narrow; labium long, reaching 16.x.2008 & 11.vi.2009; 1?, same data except for or exceeding apex of metacoxa; pronotum brownish date & collectors: 19-20. viii. 2008, T. Yasunaga & to fuscous, with finely upturned anterior margin, B. Shishido; 1?, same data except for date & collec- lacking collar; hemelytron bicolorous, sometimes tor, 26.ii.2009, T. Yasunaga. with minute spots; membrane with one or two cells (Figs 18, 19); metafemur with nine trichobothria; Diagnosis tarsi two-segmented (Figs 20, 21); claw with a tiny Recognized by the smallest body size among conge- subapical tooth; parameres conspicuously asymmet- ners, fuscous pronotum with pale posterior angles rical (right paramere usually very tiny); vesica simple, and an anterior crescent suture, elongate left para- sometimes with several spinulate appendages; phal- mere sensory lobe, extremely tiny right paramere, lotheca fused with phallobase. and apical spines on the vesica.

Distribution Description Old World tropics, subtropics and warm temper- Male. Body generally brownish, ovoid, tiny in size; ate zone; Pacific Islands, Saudi Arabia, southwest- dorsal surface brown to chocolate brown, subshin- ern Japan, Thailand. Schuh (1976) also indicated ing, with uniformly distributed, simple, semierect the occurrence of some undescribed species in New setae (Figs 1–3). Head whitish brown, almost circu- Guinea and the Philippine Islands. lar in frontal view; eyes large; vertex infuscate, about 1/5 as wide as head including eyes; apical half of tylus slightly tinged with red. Antenna dark brown; base

Downloaded from Brill.com09/25/2021 05:22:14AM via free access Yasunaga et al.: First record of Psallopinae from Thailand 95 and apex of segment I, and extreme apices of seg- lected at light, no information is currently available ments II and III creamy white (but fading to pale on the biology. Collection records suggest this psal- brown in dried specimens); segment II pale brown lopine has two or three generations per year; the mesially, a little less than head width across eyes. adults were collected in February, June, August and Labium shiny brown, slender, extending much October. beyond apex of metacoxa, reaching abdominal sternum VIII. Pronotum dark brown, with a narrow, Psallops fulvioides Yasunaga & Yamada, sp. n. transverse, crescent suture along calli; posterola- Figs 3–8, 11–17, 19, 21 teral angles of pronotum pale brown; mesoscutum and scutellum brown to chocolate brown; pleura Type material. Holotype /, Thailand: Nakhon pale brown. All coxae and basal parts of all femora Ratchasima Prov., Wang Nam Khieo Dist., Sakaerat widely dark brown; apical ½–⅓ of each femur, and Environmental Research Station, N14°30’48.6” all tibiae including spines and tarsi pale brown; tarsi E101°56’12.4”, 356m alt., under bark of a fabaceous two-segmented. Hemelytron brown to chocolate broadleaf, 13. vi. 2009, T. Yasunaga. brown, a little roughened or shagreened; anterior Additional specimens examined. 1 fourth and 1 final half and apical corner of corium, and anterior half instar nymphs, same data as for holotype. of clavus whitish brown; extreme base of corium and apex of cuneus sometimes reddish; membrane pale smoky brown, with two cells (Fig. 18). Coxae and Diagnosis legs pale brown; procoxa and base to median parts Easily recognized by the comparatively large size, of each femur more or less darkened; tarsi short, fuscous dorsal surface with two pairs of white spots two-segmented (Fig. 20). Abdomen shiny dark on the shiny fuscous hemelytra, comparatively shiny brown. Male genitalia (Figs 22–27): Genital seg- pronotum, a single membrane cell, and reddish tho- ment simple (Figs 23–24); left paramere projected racic pleurites and ventral surface of the abdomen. basally, with elongated, slender hypophysis (Figs 22, The fourth and final instar immature forms are rec- 25); right paramere reduced, very tiny (Figs 23, 26). ognizable by the elongate-oval body with sparsely Vesica bilobed, with three apical spines (Figs 23, distributed, long, elect setae, orange brown colora- 24, 27). tion, dark wingpads with creamy white apices, and Female. Unknown. reddish brown apical part of the abdomen. Measurements. Total body length 2.13–2.20; head width across eyes 0.51–0.56; vertex width 0.11– Description 0.12; lengths of antennal segment I–IV 0.12–0.15, Adult. Female: Body oval, generally fuscous; dorsal 0.48–0.51, 0.36–0.38, 0.27–0.34; labial length surface shining, with uniformly distributed, sim- 1.27–1.32; mesal pronotal length 0.26–0.29; basal ple, semierect setae (Fig. 4). Head shiny fuscous, pronotal width 0.76–0.81; width across hemelytron subvertical; vertex ⅓ times as wide as head includ- 0.84–0.87; lengths of metafemur, tibia and tarsus ing eyes; apical part of tylus slightly tinged with red 0.78–0.84, 1.08–1.14, 0.28–0.33. (Fig. 5). Antenna almost entirely dark brown; segment II pale brown at extreme apex, greater than Etymology head width across eyes; segment IV with a pale ring Named after the type locality, Sakaerat in Wang mesially. Labium dark brown, sharpened towards Nam Khieo District, northeastern Thailand; a noun apex, long, slender, reaching abdominal sternum in apposition. VIII; segments II and III pale brown. Pronotum shiny fuscous; callus indistinct; pleura partly red- Distribution dish brown. Hemelytron fuscous, with two pairs of Thailand (Nakhon Ratchasima Province). white spots (Fig. 4); membrane smoky brown, with a single cell (Fig. 19). Coxae and legs pale brown, Remarks partly tinged with red or orange; procoxa, basal parts This new species is distinguished from congeners of pro- and mesofemur, and almost entire metafe- by the smallest body size (less than 2.2 mm in total mur dark brown; extreme apex of metafemur orange lengths), creamy white apices of the dark antennal brown; metatibia almost equal in length and thick- segments II and III, dark pronotum with the pale ness to labium; tarsi long, two-segmented (Fig. 21). posterior angles and a narrow, crescent suture along Abdomen widely orange brown, except for darkened the calli, elongated left paramere sensory lobe, and genital segments (Fig. 11). Male: Unknown. extremely tiny right paramere. Fourth instar nymph (Figs 6, 15–17). Body generally Because all currently available specimens were col- pale orange brown, elongate oval, subparallel-sided;

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corium corium 0,2 mm 0,2 mm 0,2 mm

0,2 mm cuneus cuneus membrane membrane

18 19 20 21 0,1 mm

vesica

left paramere

right paramere 24 0,1 mm 0,1 mm

Figs 18–24. Hemelytral membrane (18-19), metatarsus (20-21), left paramere (22), and genital segment with expanded vesica (23-24) of Psallops sakaerat (18, 20, 22-24) and P. fulvioides (19, 21).

dorsal surface shiny, with sparsely distributed, sim- white apices (Fig. 6; in alcoholic specimen these are ple, erect setae. Head smooth; eyes small; vertex with fading to pale brown as in Fig. 15). Leg pale orange a sanguineous, V-shaped mark. Antenna brown; seg- brown; basal half of each femur and extreme apex of ment I pale reddish brown; segment II as long as III; metafemur brown; all tibiae brown, with pale brown segment IV with a pale ring mesially, slightly longer spines. Abdomen red anteriorly and posteriorly, with than III. Labium pale brown, long, reaching abdom- rather densely distributed, simple, erect setae; terga inal sternum VIII; segments III and IV darkened. VI–IX darkened mesally. Pronotum with sanguineous basal margin; meso- Final instar nymph (Figs 7, 8, 12–14): Similar in gen- and metathoracic wingpads castaneous brown, with eral features to 4th instar. Body subparallel-sided;

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Biology Thanks to the finding of a female adult and two immature specimens described above, the habitat and the 4th and final instars of the Psallopinae are herein reported for the first time. These three individuals (siblings?) were found almost simultaneously under half-detached bark fragments of a fabaceous broadleaf (Fig. 9). Numerous cracks were observed 25 on the bark surface of this tree, thus each bark frag- ment is easily peeled off. Because no other psallopine specimens were found, we could not obtain further biological information. Six species of the subfamily Isometopinae, including some immature forms, are documented to pre-

0,1 mm fer a similar habitat on an ash, Fraxinus griffithii C.B. Clarke, in Japan (Yasunaga 2005). Many isometopines are considered to be bark-inhabitants and to 26 27 prey on scale insects or other tiny arthropods (Wach- mann et al. 2004, Wheeler & Henry 1978). Based Figs 25–27. Male genitalia of Psallops sakaerat. on the similar habitat preferences, the psallopines – 25, left paramere; 26, right paramere; 27, vesica. are assumed to be also predaceous. Although both the Isometopinae and Psallopinae still require further field observations, the present discovery at least supports a close phylogenetic relationship between vestiture of dorsal surface denser. Antenna dark these two subfamilies, which has been believed since brown; segment I and mesial ring of segment IV Schuh (1976). pale brown; segment II as long as head width across In addition, the nymphs of this new Psallops species eyes; segment III slightly longer than IV. Meso- and at first sight remind us of a certain members in the metathoracic wingpads more infuscate, with clearly cylapine genus Fulvius Stål. The similarity may pre- white apices (Figs 7 & 8) that are fading to pale dict a lineage between isometopines, psallopines and brown in alcoholic specimen (Fig. 12). Abdominal fulviines. terga IV–IX darkened mesally. Measurements. Adult (/): total body length 3.16; Remarks head width across eyes 0.62; vertex width 0.20; This new species is similar in overall appearance to lengths of antennal segment I–IV 0.22, 0.79, 0.56, the Japanese P. yaeyamanus Yasunaga, from which it 0.46; labial length 1.83; mesal pronotal length 0.48; is readily distinguished by the mesial pale ring on basal pronotal width 1.21; width across hemelytron the dark antennal segment IV, fuscous hemelytron 1.32; lengths of metafemur, tibia and tarsus 1.20, that is provided with two pairs of white marks and 1.80, 0.44. Nymphs (4th/ 5th): total body length lacks dark spots on the pale regions, and a single 2.15/ 2.55; head width across eyes 0.51/ 0.57; membrane cell. Such single-celled membrane is also lengths of antennal segment I–IV 0.17, 0.38, 0.38, reported in P. oculatus Usinger from Guam Island 0.42/ 0.19, 0.57, 0.51, 0.50; labial length 1.54/ (Carvalho 1956). The size and coloration are greatly 1.80; basal pronotal width 0.57/ 0.71; width across different from the other new species described in the wingpads 0.76/ 0.99; lengths of metafemur, tibia present paper, however. and tarsus 0.66, 0.78, 0.30/ 0.95, 1.14, 0.57.

Etymology Acknowledgements Named after the generic name Fulvius Stål of the Special thanks are due to Dr S. Miyamoto (Fuku- subfamily Cylapinae as the present new species at oka, Japan) for continuous advice and encourage- first sight resembles a certain species of this cylapine ment. We are also much indebted to the following genus; an adjective. individuals for supporting our field investigations: Dr P. Joompot and Assoc. Prof. P. Ampol (Rajaman- Distribution gala University of Technology Suvarnabhumi), and Thailand (Nakhon Ratchasima Province). Mr B. Shishido (Himeji, Japan). Thanks are extended

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to Dr R.T. Schuh (AMNH) and Dr E.J. van Nieu- Wachmann, E., A. Melber. & J. Deckert, 2004. Wanzen. kerken (Natural History Museum Naturalis, Leiden) 2. Cimicomorpha: Microphysidae (Flechtenwanzen), for improving the manuscript with kind comments Miridae (Weichenwanzen). Neubearbeitung der Wan- and suggestions. This study was partly supported zen Deutschlands, Österreichs und der deutschspra- by an international cooperative program between chigen Schweiz. – Die Tierwelt Deutschlands 75: JICA (Japan International Cooperation Agency) 1–288. Goecke & Evers, Keltern. Wheeler, A.G., Jr., 2001. Biology of the Plant Bugs and Rajamangala University of Technology Suvar- (Hemiptera: Miridae), Pests, Predators, Opportun- nabhumi, and Grant-in-Aid for Young Scien- ists, xv+507 pp. – Cornell University Press, Ithaca & tists (B) from the Japan Ministry of Education, London. Culture, Sports, Science and Technology to KY Wheeler, A.G., Jr. & T.J. Henry, 1978. Isometopinae (No. 20780043). (Hemiptera: Miridae) in Pennsylvania: Biology and descriptions of fifth instars, with observations of pre- dation on obscure scale. – Annals of the Entomologi- References cal Society of America 71: 607–614. Carvalho, J.C.M., 1956. Insects of Micronesia: Miridae. Yasunaga, T., 1999. First record of the plant bug subfamily – Bernice P. Bishop Museum, Honolulu 7: 100 pp. Psallopinae (Heteroptera: Miridae) from Japan, with Kerzhner, I.M. & M. Josifov., 1999. Miridae Hahn, 1833. descriptions of three new species of the genus Psallops - In Aukema, B. & C. Rieger (eds.), Catalogue of the Usinger. – Proceedings of the Entomological Society Heteroptera of the Palearctic Region, vol. 3, Cimico- of Washington 101: 737–741. morpha II, 1–576 pp. – The Netherlands Entomo- Yasunaga, T., 2001. Family Miridae Hahn, plant bugs. - In logical Society. Yasunaga T., M. Takai & T. Kawasawa (eds.). A Field Linnavuori, R. & K.T. Alamy, 1982. Insects of Saudi Guide to Japanese Bugs II, pp. 112–276. – Zenkoku Arabia. Hemiptera. – Fauna of Saudi Arabia 4: 89–98. Noson Kyoiku Kyokai Publ. Co. Ltd., Tokyo. Schuh, R.T., 1976. Pretarsal structure in the Miridae Yasunaga, T., 2005. Isometopine plant bugs (Heteroptera: (Hemiptera) with a cladistic analysis of relationships Miridae), preferably inhabiting Fraxinus griffithii on within the family. – American Museum Novitates Ishigaki Island of the Ryukyus, Japan. – Tijdschrift 2601: 1–39. voor Entomologie 148: 341–349. Schuh, R.T., 1995. Plant bugs of the world (Insecta: Het- eroptera: Miridae). Systematic catalog, distributions, host list and bibliography. xii+1329 pp. – The New York Entomological Society. [Continuing updated catalogue available on webpage: http://research.amnh. org/pbi/catalog/] Usinger, R.L., 1946. Hemiptera Heteroptera of Guam. In: Insects of Guam. II. – Bulletin of the Bishop Museum. Received: 30 October 2009 189: 11–103. Accepted: 25 January 2010

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