Discovery of a Cryptic Termite Genus, Stylotermes (Isoptera: Stylotermitidae), in Taiwan, with the Description of a New Species

Annals of the Entomological Society of America, 110(4), 2017, 360–373 doi: 10.1093/aesa/sax034 Advance Access Publication Date: 23 March 2017 Research Research article

Discovery of a Cryptic Termite Genus, Stylotermes (Isoptera: Stylotermitidae), in Taiwan, With the Description of a New Species

Wei-Ren Liang, Chia-Chien Wu, and Hou-Feng Li1

Department of Entomology, National Chung Hsing University, 145 Xingda Rd., Taichung 40227, Taiwan ([email protected]; [email protected]; [email protected]), and 1Corresponding author, e-mail: [email protected] Subject Editor: Allen Szalanski

Received 18 October 2016; Editorial decision 11 January 2017

Abstract The termite family Stylotermitidae consists of a single extant genus, Stylotermes, present only in eastern Asia. Stylotermes has distinctively trimerous tarsi and is considered an intermediate between the Rhinotermitidae and Kalotermitidae families. The present study reports the ﬁrst discovery of the Stylotermitidae family in Taiwan. On the basis of a comparison between the Taiwanese samples and the original descriptions of all the other 44 Stylotermes species, a new species collected from eastern Taiwan is described as Stylotermes halumicus sp. nov. This study is the ﬁrst to report the gene sequence and detailed morphological descriptions of the winged imago, soldier, and worker of a single Stylotermes sp. Furthermore, a preliminary review of the Stylotermes taxonomy is provided.

Key words: Stylotermitidae, wood-feeding termite, Taiwan, 16S, COII

Holmgren and Holmgren (1917) established a new genus, Malaysia. In China, 35 Stylotermes spp. were described between Stylotermes, as the type genus of the new Stylotermitinae subfamily 1963 and 1993 from eight provinces: Fujian [no. of spp. (n) ¼ 2], of the Rhinotermitidae family. On the basis of the morphology of Guangdong (n ¼ 2), Guangxi (n ¼ 4), Guizhou (n ¼ 4), Hainan winged imago and soldier castes, Stylotermes was speculated to be (n ¼ 3), Hunan (n ¼ 1), Sichuan (including Chongqing city; n ¼ 16), the most primitive living taxon in Rhinotermitidae and to be an inter- and Yunnan (n ¼ 3). In addition, Ping (2000) provided the soldier mediate between Rhinotermitidae and Kalotermitidae (Holmgren identification key of these Chinese species. and Holmgren 1917). Chatterjee and Thakur (1964) elevated the sub- Although 44 Stylotermes spp. have been described to date, the family Stylotermitinae to a familial status by highlighting the impor- taxonomy of Stylotermes remains controversial. Descriptions of the tance of the distinctive trimerous tarsi of Stylotermitidae. However, Chinese species were too brief and thus insufficient for species identi- several researchers have continued to consider Stylotermitidae as a fication. In addition, all descriptions of the Chinese species were pub- subfamily of Rhinotermitidae (Krishna 1970, Emerson 1971, Akhtar lished in Chinese. To date, Stylotermes has been excluded from 1975), whereas other researchers have considered it with its familial molecular phylogeny because their specimens were unavailable for status (Roonwal 1975, Chhotani 1984, Engel et al. 2009). sequencing (Inward et al. 2007, Ware et al. 2010, Bourguignon et al. Furthermore, morphological analysis by Ware et al. (2010) revealed 2015). The slow progress regarding the study of the Stylotermes ge- Stylotermitidae to be nested within the Rhinotermitidae family. To nus is likely due to the difficulty involved in its collection procedure date, Stylotermitidae contains one living genus, Stylotermes, and two (Yu and Ping 1964). The natural history of Stylotermes is similar to fossil genera, Parastylotermes Snyder and Emerson, 1949 and that of some genera in the Kalotermitidae family (e.g., Neotermes Prostylotermes Engel and Grimaldi, 2011 (Krishna et al. 2013). and Glyptotermes), which were found dwelling in the dead portion of Stylotermes, an eastern Asian genus, is found in Bangladesh, a living tree (Chhotani and Bose 1979). Their nest comprised longitu- China, India, and Malaysia (Krishna et al. 2013), and the original dinal, irregular, and narrow galleries in the branches and stems of the descriptions of the corresponding species are presented in Fig. 1. living trees (Chatterjee and Thakur 1963). Holmgren and Holmgren (1917) described the first Stylotermes spe- In Taiwan, the termite fauna has been studied since the early cies, S. fletcheri, from Karnataka, India. To date, seven species have twentieth century (Oshima 1912, Hozawa 1915, Tu 1955, Chung been described from India. Akhtar (1975) described S. ahmadi from and Chen 1994, Tsai 2003, Zhu 2005). Currently, taxonomic and di- Bangladesh, and Thapa (1982) described S. roonwali from Sabah, versity studies are ongoing in the Laboratory of Urban Entomology,

VC The Authors 2017. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please email: [email protected] Version of Record, first published online March 23, 2017 with fixed content and layout in compliance with Art. 8.1.3.2 ICZN. 360 Downloaded from https://academic.oup.com/aesa/article-abstract/110/4/360/3076965/Discovery-of-a-Cryptic-Termite-Genus-Stylotermes by National Chung Hsing University Library user on 25 August 2017 Annals of the Entomological Society of America, 2017, Vol. 110, No. 4 361

Fig. 1. Type localities of 45 Stylotermes species worldwide based on original descriptions. 1, S. acrofrons Ping and Liu, 1981;2,S. ahmadi Akhtar, 1975;3,S. alpi- nus Ping, 1983;4,S. angustignathus Gao, Zhu, and Gong, 1982;5,S. beesoni Thakur, 1975;6,S. bengalensis Mathur and Chhotani, 1959;7,S. chakratensis Mathur and Thapa, 1963;8,S. changtingensis Fan and Xia, 1981;9,S. chengduensis Gao and Zhu, 1980; 10, S. chongqingensis Chen and Ping, 1983; 11, S. choui Ping and Xu, 1981; 12, S. crinis Gao, Zhu, and Gong, 1981; 13, S. curvatus Ping and Xu, 1984; 14, S. dunensis Thakur, 1975; 15, S. faveolus (Chatterjee and Thakur, 1964); 16, S. ﬂetcheriHolmgren and Holmgren, 1917; 17, S. fontanellus Gao, Zhu, and Han, 1982; 18, S. guiyangensis Ping and Gong, 1984; 19, S. hanyuanicus Ping and Liu, 1981; 20, S. inclinatus (Yu and Ping, 1964); 21, S. jinyunicus Ping and Chen, 1981; 22, S. labralis Ping and Liu, 1981; 23, S. laticrus Ping and Xu, 1981; 24, S. latilabrum (Tsai and Chen, 1963); 25, S. latipedunculus (Yu and Ping, 1964); 26, S. lianpingensis Ping, 1983; 27, S. longignathus Gao, Zhu, and Han, 1981; 28, S. mecocephalus Ping and Li, 1978; 29, S. minutus (Yu and Ping, 1964); 30, S. mirabilis He and Qiu, 1990; 31, S. orthognathus Ping and Xu, 1984; 32, S. parabengalensis Maiti, 1975; 33, S. planifrons Chen, 1984; 34, S. robustus Ping and Li, 1981; 35, S. roonwali Thapa, 1982; 36, S. setosus Li and Ping, 1978; 37, S. sinensis (Yu and Ping, 1964); 38, S. sui Ping and Xu, 1993; 39, S. triplanus Ping and Liu, 1981; 40, S. tsaii Gao, Zhu, Yang, Ji, and Ma, 1982; 41, S. undulates Ping and Li, 1978; 42, S. valvules Tsai and Ping, 1978; 43, S. wuyinicus Li and Ping, 1981; 44, S. xichangensis Huang and Zhu, 1986; 45, S. halumicus. Plot by QGIS desktop 2.14.2.

National Chung Hsing University (NCHU; Li et al. 2008, 2009, 2015; deposited in the NCHU Termite Collection, Department of Chiu et al. 2016; Liang and Li 2016). In a follow-up investigation on Entomology, NCHU, Taichung, Taiwan. A long-term termite the termite fauna of the pangolin habitat in southeastern Taiwan (Li fauna survey was conducted in the Luanshan area during 2011– et al. 2011), we discovered a colony of Stylotermes spp. in 2014. 2016. All the termite specimens, a total of 353 termite colonies Stylotermitidae is the fifth termite family reported in Taiwan, along from 143 collection sites (Supp. Fig. 1 [online only]) in Luanshan, with Termitidae, Rhinotermitidae, Kalotermitidae, and were deposited at NCHU. Our comprehensive survey in the Archotermopsidae (Li et al. 2010). By comparing the morphological Luanshan area and other surveys conducted in the remaining areas characters of these families, we described a novel species, Stylotermes of Taiwan (H.F.L., unpublished data) indicated that Stylotermes is halumicus sp. nov., and provided the first DNA barcode (16S rRNA the most cryptic and rarest termite taxon encountered in Taiwan. and COII gene sequences) for the Stylotermitidae family. To study the biology of Stylotermes, we described the novel species on the basis of numerous soldiers and workers from one colony and an additional winged imago sample, which was collected Materials and Methods from Lide, Pingtung County. The winged imago, which was col- Soldier and worker samples of S. halumicus sp. nov. were collected by M.-L. Jeng and T.-R. Chen with a flight interception lected using a hatchet and hand saw to split the dead branch of a trap, is deposited in the National Museum of Natural Science living Zelkova serrata (Thunb.) in Luanshan, Taitung County, (NMNS), Taichung, Taiwan. By comparing the mitochondrial Taiwan (22.9139 N, 121.1839 E); the samples were preserved gene sequences, we confirmed that worker, soldier, and winged in 95% ethanol. Specimens, except for type specimens, were imago samples used for species description are the same species.

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We selected 21, 19, and 12 quantitative characters of a winged coated with gold, and images were obtained using a scanning imago, soldier, and worker, respectively, on the basis of the de- electron microscope (TM3000 Tabletop scanning electron micro- scriptions of the 44 Stylotermes spp. (Tables 1 and 2). scope, Hitachi, Tokyo, Japan) at 15 kV. Photographs were cap- Measurements were recorded using a Leica M205 C stereomicro- tured by the Leica MC170 HD digital camera or a Canon EOS scope and a Leica MC170 HD digital camera with LAS software 760D with a micro lens (Canon Inc., Tokyo, Japan) and subse- (version 4.4.0, Leica Application Suite, Wetzlar, Germany). quently combined by the automontage software CombineZP Morphological measurements were conducted according to the (Hadley 2010). Contrast-enhanced SEMs and photographs were criteria by Roonwal (1969). The color of the samples were evalu- obtained using Adobe Photoshop CS6 (Adobe Systems Software ated using the microscope and the observations were comparted Ireland Ltd, Dublin, Ireland), and backgrounds were converted with the Munsell color system (Munsell Color Company 1975, into black or white. Line drawings were illustrated using the KellyandJudd1976) to determine hue, value, and chroma of Leica DM750 microscope with the help of a drawing tube each described character. Morphological characters were demon- attachment. strated by scanning electron micrographs (SEMs), photographs, The novel species, S. halumicus sp. nov., was confirmed by and line drawings. Specimens for SEMs were dehydrated in 95% comparing the morphometric and qualitative characters of the and 99.5% ethanol. The dehydrated specimens were sputter- soldier with those of the other 44 described species. Six com- monly measured characters with less artificial deviation are the maximum width of the head [no. of species with this measurement (n) ¼ 45], height of the head (n ¼ 43), maximum width of Table 1. Measurements of soldier of Stylotermes halumicus the labrum (n ¼ 43), maximum width of the pronotum (n ¼ 45), Measurement (mm) Stylotermes halumicus length of the hind femur (n ¼ 35), and length of the hind tibia (n ¼ 37). Hence, 34 species were compared with S. halumicus sp. Range Mean 6 SD nov. based on these six characters, two (S. undulates and S. val- Length at head including mandibles 3.43–3.99 3.71 6 0.14 vules) were compared based on five characters, five (S. beesoni, Length of head-capsule 2.23–2.61 2.45 6 0.09 S. chakratensis, S. faveolus, S. parabengalensis,andS. setosus) Maximum width of head 1.34–1.50 1.44 6 0.04 were compared based on four characters, two (S. dunensis and Width of fontanelle 0.01–0.05 0.03 6 0.01 S. roonwali) were compared based on three characters, and one Length of left mandible 1.50–1.64 1.58 6 0.04 (S. fletcheri) was compared based on two characters. When all of Maximum length of postmentum 1.62–1.95 1.78 6 0.10 these available measurements of one species overlapped with Maximum width of postmentum 0.53–0.63 0.57 6 0.02 those of S. halumicus sp. nov., this species was considered as a Minimum width of postmentum 0.18–0.22 0.20 6 0.01 similar species. Furthermore, qualitative characters of the similar Maximum length of labrum 0.32–0.46 0.36 6 0.04 species and S. halumicus sp. nov. were compared. Maximum width of labrum 0.39–0.44 0.41 6 0.02 Maximum length of pronotum 0.67–0.82 0.76 6 0.05 The termite workers used for molecular sequencing were pre- Median length of pronotum 0.55–0.67 0.62 6 0.03 served in 95% ethanol. Genomic DNA was extracted from the tho- Maximum width of pronotum 1.10–1.34 1.24 6 0.06 rax muscle tissue of the workers by using the DNA Extraction Kit Maximum width of mesonotum 0.84–0.99 0.95 6 0.04 (BuccalAmp, Epicentre, Madison, WI). Partial mitochondrial 16S Maximum width of metanotum 0.91–1.05 1.01 6 0.03 rRNA and COII gene sequences were amplified through polymerase Length of hind femur 0.89–1.06 0.98 6 0.05 chain reaction (PCR) with 16S1260-F3 (50-TTTAATCCAAC Width of hind femur 0.37–0.49 0.44 6 0.05 ATCGAGGT-30), 16S870-R3 (50-AGCCGCAGTATTTTGACTGT- Length of hind tibia 0.91–1.15 1.07 6 0.05 30), COII-TE-3058F (50-TAAGCTCCACAYATAAAGT-30), and Segments of antenna 12–14 COII-TE-3770R (50-GTCATCTGATGATTCTCTTAG-30). The total 25.3-ll PCR mixture of 16S rRNA and COII gene sequences n ¼ 19, from one colony. contained 19.8 llofddH2O,0.5ll of dNTP mixture (25 mM), 0.5 ll of Taq DNA polymerase, forward and reverse primers (0.5 ll each, 10 mM), 2.5 ll of 10X reaction buffer, and 1 llofthe termite DNA template. PCR thermal cycling reaction included a Table 2. Measurements of worker of Stylotermes halumicus predenaturation process at 94 Cfor2min,followedby35cycles Measurement (mm) Stylotermes halumicus of denaturation at 94 C for 40 s, annealing at 55 Cfor1min, and extension at 72 C for 40 s, and then a post extension at 72 C Range Mean 6 SD for 10 min. The two DNA sequences are available in the GenBank Length of head to tip of labrum 1.17–1.50 1.32 6 0.11 (accession numbers, KX858796 and KX858797). The worker and Maximum width of head 1.05–1.26 1.16 6 0.07 winged imago samples were also sequenced using the next- Height of head 0.60–0.85 0.74 6 0.76 generation sequencing method to obtain mitochondrial genomes Maximum length of labrum 0.29–0.40 0.35 6 0.03 (H.F.L., unpublished data). Maximum width of labrum 0.35–0.43 0.39 6 0.25 Maximum length of pronotum 0.35–0.56 0.47 6 0.06 Median length of pronotum 0.30–0.48 0.39 6 0.05 Maximum width of pronotum 0.72–0.96 0.85 6 0.08 Nomenclature Length of hind femur 0.49–0.76 0.66 6 0.08 This paper and the nomenclatural act(s) it contains have been regis- Width of hind femur 0.14–0.28 0.23 6 0.04 tered in Zoobank (www.zoobank.org), the official register of the Length of hind tibia 0.56–0.82 0.67 6 0.07 Segments of antenna 14–16 International Commission on Zoological Nomenclature. The LSID (Life Science Identifier) number of the publication is: urn:lsid: n ¼ 11, from one colony. zoobank.org:pub:6A152A3E-B051-4AA5-9960-0839845D49FC

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Fig. 2. Habitus and head of winged imago of Stylotermes halumicus. Body habitus (A). Head in dorsal (B), oblique (C), and lateral (D) views. Scale bar is 1 mm.

STYLOTERMITIDAE K. Holmgren and N. Diagnosis Holmgren, 1917 Winged Imago Genus Stylotermes K. Holmgren and N. Holmgren, 1917 Fontanelle present in Stylotermes and Rhinotermitidae, but that ab- Type species: Stylotermes fletcheri K. Holmgren and N. Holmgren, sent in Kalotermitidae. Tarsi formula of Stylotermes is 3:3:3, and 1917. that of Rhinotermitidae and Serritermitidae is 4:4:4. Tibial spurs OperculitermesYu and Ping, 1964: 345, 359–360. formula of the three genera of Stylotermitidae, Stylotermes, Sarvaritermes Chatterjee and Thakur, 1964: 149–151. Parastylotermes, and Prostylotermes, are 3:2:2, 2:2:2, and 2:2:2,

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Fig. 4. Wings of Stylotermes halumicus. Forewing (A) and hindwing (B). Scale bar is 1 mm.

slightly concave or straight. Tibial spurs formula 3:2:2. Tarsi formula 3:3:3.

Soldier Head rectangular or oval rectangular. Head capsule highly sclero- tized, red-brown. Eye of most species vestigial or absent; few species’ eye present. Fontanelle located at middle of the head. Mandible acinaciform, incurved apically. Inner margin of mandible with tiny crenulation or smoothed. Outer margin of mandible smoothed or wavy. Labrum linguiform. Pronotum trapezoid. Anterior margin with V-shape concave; posterior margin slightly concave or straight in the middle. The third segment of antenna broadest at apex. Tibial spurs formula 3:2:2. Tarsi formula 3:3:3.

Worker Head subcircular. Labrum linguiform. Mandible with one apical, three marginal teeth, and a molar tooth. The second marginal tooth of left mandible vestigial. Anterior margin of pronotum slightly concave; posterior margin emarginated or smooth. Tibial spurs 3:2:2. Tarsi formula 3:3:3.

Biological Notes Stylotermes species were recorded as wood-feeding termites, living in dead wood or living trees. According to 34 species noted with host tree species or genus in their original descriptions, we speculated Stylotermes spp. prefer infesting living trees. One of these spe-

Fig. 3. Pronotum and legs of winged imago of Stylotermes halumicus. cies, S. faveolus, was further reported to attack aged healthy trees Pronotum (A). Right foreleg (B). Left hindleg (C). Scale bar is 0.5 mm. (Chatterjee and Thakur 1963).

Distribution respectively. Antennae segments of Stylotermes, Parastylotermes, Oriental region (Fig. 1): Bangladesh, China, India, Malaysia and Prostylotermes are 18-22, 16-17, and 17, respectively. (Krishna et al. 2013), and Taiwan (newly recorded country in this study). Soldier Head shapes of Stylotermes and that of Glyptotermes of Kalotermitidae are similar, but fontanelle present in Stylotermes, not Stylotermes halumicus Liang, Wu, and Li sp. nov. Kalotermitidae. Inner margins of mandible of Stylotermes is 5 species nova 5 new species smoothed or much less serrated than that of Serritermitidae. Tarsi (urn:lsid:zoobank.org:act:88B6390E-6676-41BF-B14E-78FB35D8F280) formula of Stylotermes is 3:3:3, and that of Rhinotermitidae is 4:4:4. HOLOTYPE: a soldier collected at TAIWAN: Taitung Co.: Luanshan: 22.9139 N, 121.1839 E; 605 m; 3-IX-2014; W.-R. Description Liang (TW5080), deposited in NMNS. Winged Imago PARATYPE: a female winged imago collected at TAIWAN: Head circular or subcircular. Some part of Y-suture invisible or ob- Pingtung Co.: Lide: 22.0193 N, 120.8618 E; 208 m; 4-VII- scure. Mandible with one apical tooth, three marginal teeth, and 200914-VII-2009; by flight interception trap; M.-L. Jeng and T.- one molar tooth. The second marginal tooth of left mandible vesti- R. Chen, deposited in NMNS. 7 soldiers; the same colony as gial. Anterior margin of pronotum emarginated; posterior margin Holotype (TW5080), deposited in NCHU. 11 soldier, locality same

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Fig. 5. Soldier head of Stylotermes halumicus. Head in dorsal (A), ventral (B), and lateral (C) views. Labrum in dorsal view (D). Pits on the juncture of postclypeus and frons (E and F). Fontanelle (G and H). Scale bars in A, B, and C are 1 mm and the others are 0.1 mm.

as Holotype; 13-XI-2015; H.-F. Li, C.-I. Chiu, and W.-R. Liang head longer than broad. Epicranial suture invisible. Capsule covered (TW5238), deposited in NCHU. with several setae. Antennae (Fig. 2B) with 17 segments; first and second sparsely hairy, the others hairy; first thickest, broadest at apex; second cylindrical, shorter than first; third the shortest; 4th to Winged Imago (Figs. 2–4) 10th moniliform, 11th to the second-last antennomere turbinate, Descriptions were based on one single winged imago. Head capsule gradually increase in length to apex; the last antennomere elongate moderate reddish brown (10R 3/6). Head (Fig. 2) oval, length of oval. Labrum moderate yellow (2.5Y 8/6), linguiform, broader than

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Fig. 6. Soldier mandibles of Stylotermes halumicus. Mandibles in dorsal (A) and ventral (B) views. Base of left mandible in dorsal view (C) with numerous short setae. Central area of left mandible in ventral view (D) with tiny crenulations. Scale bars in A and B are 0.5 mm and the others are 0.1 mm.

length; posterior margin concave, anterior margin with two long se- Leg (Fig. 3) pale yellow (2.5Y 8/4), femur stout, length about tae, central area with four long setae and some short setae. three times as width, shorter than tibia. Tibia slender, tibial spurs Postclypeus trapezoidal, with six long setae. Anteclypeus whitish, formula 3:2:2, tarsi 3-jointed. Forewing scale with about 20–30 se- trapezoidal. Eye circular. Ocelli suboval (rice shape-like). Pronotum tae; membrane without hairs (Fig. 4A). Forewing scale about two (Fig. 3) moderate orange (5YR 6/8), broadest at middle, anterior times wider than hindwing scale, forewing scale overlapping the margin middle notched; lateral margin converging posteriorly; pos- base of hindwing scale (Fig. 2A); costa and radius sclerotic, close to teriorly margin concave, covered with 10–20 long setae and 20–40 each other, and connect by small veinlets. Median and cubitus run- short setae; entire margin fringe with 30–40 long setae. Abdomen ning parallel to each other. Cubitus with 22 branches. Hindwing (Fig. 2A) oblong, hairy. (Fig. 4B) similar as forewing. Body length with wings 10.59 mm;

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Fig. 7. Soldier antenna of Stylotermes halumicus. Right antenna in dorsal view (A). Right antenna in ventral view (13th segment lost) (B). Base of antenna in dorsal view (C). Scale bars are 0.5 mm.

body length 5.42 mm; maximum head length 1.38 mm; maximum head width 1.30 mm; head height 0.82 mm; labrum length 0.32 mm; labrum width 0.39 mm; pronotum length 0.63 mm; pronotum middle length 0.56 mm; pronotum width 1.06 mm; forewing length 7.80 mm; hindwing length 7.47 mm; hind femur length 0.82 mm; hind femur width 0.28 mm; hind tibia length 0.28 mm; maximum compound eye diameter 0.36 mm; minimum compound eye diameter 0.33 mm; maximum ocellus diameter 0.15 mm; minimum ocellus Fig. 8. Soldier pronotum and abdomen of Stylotermes halumicus. Pronotum diameter 0.08 mm; minimum eye-ocellus distance 0.05 mm; distance (A) and abdomen (B) in dorsal view. Scale bar is 1 mm. between compound eye to head capsule margin 0.10 mm.

and some (5–10) short (< 0.1 mm) setae. Anteclypeus whitish, short, Soldier (Figs. 5–10; Table 1) convex anteriorly. Postclypeus indistinguishable from frons. Head capsule moderate orange (5YR 6/8), paler posteriorly. Head Fontanelle whitish, nearly oval (Fig. 5G) or oblong (Fig. 5H), lo- (Fig. 5) rectangular, flat, length longer than broad. Sides almost par- cated at anterior to middle of capsule. Two pits on the juncture of allel. Capsule cover with dense short setae (< 0.15 mm) and several postclypeus and frons (Fig. 5D–F). Mandible (Fig. 6A and B) long, long setae (> 0.2 mm). Coronal suture invisible with frontal suture stout, incurved apically, with 20–30 short setae on the dorsal surface obscure. Postmentum (Fig. 5B) long, broad anteriorly, narrow in the of the base (Fig. 6C). Inner margin of mandible with several tiny middle, anterior broader part bilobed laterally, posterior lobe wider crenulations (Fig. 6D). Left mandible with one denticle bellows mid- than anterior lobe, pilosity greater anteriorly. Frons sloping anteri- dle. Right mandible with one denticle near the base. Antenna (Fig. orly (Fig. 5C). Labrum (Fig. 5D) linguiform, broadest at middle, 7) with 12–14 segments, first and second sparsely hairy, the others posterior margin concave, anterior margin covered with 10–15 long hairy; first thickest, broadest at apex; second cylindrical, shortest; (> 0.15 mm) setae, central area with four long (> 0.15 mm) setae third the longest, broadest at apex; fourth and fifth cylindrical, sixth

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with 60–80 long setae. Mesonotum and metanotum similar in shape, narrower than pronotum, pilosity similar to pronotum. Pleural processes of mesonotum and metanotum small and sclerotic (Fig. 9A). Abdomen (Fig. 8B) oblong, hairy. Legs (Fig. 10), femur stout, suboval (rice shape-like), length as two times as width, shorter than tibia; tibia (Fig. 10C) slender, with the scaly-shaped microstructure around the basal end (Fig. 10D). Tibial spurs formula 3:2:2 (Fig. 10E), tarsi 3-jointed.

Worker (Figs. 9, 11–12; Table 2) Head capsule moderate orange yellow (10YR 8/8), subcircular, length of head to tip of labrum longer than width (Fig. 11A). Capsule cover with dense short setae (< 0.05 mm) and several long setae (> 0.1 mm). Antennae with 14–16 segments, first and second sparsely hairy, third and fourth with no setae, the others hairy (Fig. 11A–C); first thickest, broadest at apex; second cylindrical, shorter than first; third and fourth the shortest and narrowest (Fig. 11C); fifth–seventh moniliform, broader than length; eighth to the second- last antennomere turbinate, gradually increase in length to apex; the last antennomere elongate oval (Fig. 11A and B). Labrum linguiform, a little broader than its length, broadest at the middle, posterior margin concave, anterior margin covered with six long (> 0.05 mm) setae, central area with six long (> 0.05 mm) setae and some short (< 0.01 mm) setae. Anteclypeus whitish with middle area of each half side yellow (10YR 8/8), short, flat trapezoidal, convex anteriorly, glabrous. Postclypeus yellow (10YR 8/8), length as long as and broader than anteclypeus, three setae on each side. Pronotum (Fig. 11D) pale yellow (2.5Y 8/4), broadest at top quartile, anterior margin slightly concave, posteriorly gradually narrow, posterior margin emarginated, covered with several setae. Pleural processes of mesonotum and metanotum much rounded and sclerotic in large worker (Fig. 9B), and much prominent and weakly sclerotic in small worker (Fig. 9C); those on mesonotum were smaller than those on metanotum. Legs and abdomen, similar to the soldier. Mandible (Fig. 12A–C) with one apical, three marginal teeth, and a molar tooth in both large (Fig. 12A) and small (Fig. 12B) worker; some setae at base of mandible (Fig. 12D) and dorsal surface of molar tooth (Fig. 12E). Left mandible with apical tooth large, first marginal tooth triangular, smaller than apical tooth, second marginal tooth the smallest, third marginal tooth triangular, di- rected backward, as large as apical tooth, molar tooth the largest. Right mandible with apical tooth large, first marginal tooth vestigial, the smallest, second marginal tooth smaller than apical tooth, third marginal tooth bladelike, the largest, molar tooth smaller than third marginal tooth.

Fig. 9. Pleural processes of Stylotermes halumicus.Soldier(A). Large Larva (Fig. 9D) worker (head width: 1.26 mm; antenna segments: 16) (B). Small worker Nymph body whitish and unsclerotic. Pleural processes of mesono- (head width: 1.02 mm; antenna segments: 14) (C). Larva (D). p.ms: pleural processes of mesonotum; p.mt: pleural processes of metanotum. Scales tum and metanotum distinctly prominent, the former was smaller bar are 0.1 mm. than latter; pleural processes of mesonotum rounded; pleural processes of metanotum pointed and slightly bent posteriorly (Fig. 9D).

to the second-last antennomere turbinate, gradually increase in Winged Imago Comparison length to apex; the last antennomere elongate oval. Winged imagos of 10 species have been described. Winged imago of Pronotum (Fig. 8) trapezoid, width 1.5 times longer than length, S. halumicus has 17 antennae segments, while 16 segments in S. ben- narrower than width of head. Anterior margin emarginate, ante- galensis and S. wuyinicus, 20–22 segments in S. faveolus, and 18–19 lateral corner broad and rounded, lateral margin converging posteri- segments in S. fletcheri. The head length of S. halumicus is longer orly, posterior margin slightly concave in the middle. Pilosity, pro- than its width, but the head width of S. bengalensis, S. dunensis, S. notum covered with 50–70 setae (0.25–0.03 mm in length), except faveolus, S. fletcheri, S. minutus, and S. sinensis are longer than its anterior to middle of central area glabrous; entire margin fringe length. Epicranial suture of S. halumicus invisible, but the epicranial

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Fig. 10. Soldier legs of Stylotermes halumicus. Foreleg (A), midleg (B), and hindleg (C) in dorsal views. Scaly shaped microstructure around the base of foreleg tibia (D). Tibia spurs of foreleg (E). Scale bars in A, B, and C are 0.5 mm and the others are 0.1 mm.

suture of S. bengalensis, S. choui, S. faveolus, and S. wuyinicus are setae. Pronotum of S. halumicus covered with 50–70 setae, except ante- visible. The pronotum of S. halumicus with middle line, but S. rior to middle of central area glabrous, is different from the pronotum changtingensis absent. The cubitus of S. halumicus with 22 of S. chengduensis, which has central area with few and short setae, S. branches, but S. tsaii only with 16 branches. Description of S. jinyu- jinyunicus and S. planifrons, which has about 10 setae in the central nicus is too brief to compare with S. halumicus. area, S. triplanes, which has middle area with no setae, and S. wuyinicus, which has about 20 setae in the central area. Head of S. halumicus rectangular, sides almost parallel, is different from S. planifrons,which Soldier Comparison has head subrectangular, sides slightly concave in middle and promi- The result of the morphometrics comparison (Fig. 13) showed only 11 nent posteriorly, and S. wuyinicus, which has head rectangular, sides of 44 Stylotermes species were not differentiable from the Taiwanese slightly prominent posteriorly. Mandible of S. halumicus long, stout, sample, but it can be further distinguished with these 11 species based incurved apically, is different from S. angustignathus, which has basal on five qualitative characters: eye, setae of labrum, setae of pronotum, margin of mandible slightly wavy, S. chengduensis, which has right shape of head capsule, and shape of mandible. Based on the original de- mandible smaller and its inner margin straighter than left mandible, S. scriptions and morphological figures, the eye of S. halumicus vestigial, jinyunicus, which has outer margin of mandible slightly concave, S. lat- but the eye of S. chengduensis, S. dunensis,andS. triplanus are present. ipedunculus and S. sinensis, which has left and right mandible asym- Five to ten short setae and four long setae on the central area of labrum metrical and outer margin irregularly wavy. Consequently, Stylotermes of S. halumicus, which is different from S. angustignathus with seven halumicus do not correspond to any other descriptions of Stylotermes to eight short setae and S. valvules with two long setae and two short species, and we described it as new species in this study.

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Fig. 12. Worker mandibles of Stylotermes halumicus. Mandibles of large worker (head width: 1.23 mm) (A) and small worker (head width: 1.05 mm) (B) in dorsal view. Mandibles of worker (head width: 1.15 mm) (C) in ventral view. Base of left mandible (D) and molar tooth of left mandible in dorsal view (E). Scale bars are 0.1 mm.

caste, like larva and small worker, while the pleural processes of the soldier were indistinct and almost sclerotic. Fig. 11. Worker of Stylotermes halumicus. Worker head in dorsal (A) and lateral (B) views. Basal end of antenna (C). Pronotum in dorsal view (D). Scale bar in C is 0.1 mm and the others are 0.5 mm. Taxonomic Notes According to original descriptions, the species delimitation of Morphological Notes Stylotermes species were mainly based on soldier caste. The quan- Pleural processes of Stylotermes were only described in S. fletcheri titative characters had been used for species delimitation. (Holmgren and Holmgren 1917). Roonwal (1975) confirmed the oc- Morphometrics of the soldier of 44 described species were listed currence of pleural processes in S. fletcheri, and absence in the other in Supp. Table 1 (online only). Most species were described base species. The descriptions of rest species do not mention these pro- on only one colony (39 of the 45 species), and the maximum sam- cesses, and cannot confirm their presence or not. In S. halumicus sp. ple size of one single species is five colonies. The rare occurrence nov., pleural processes were more distinct and prominent in young and uncertain special identification character of Stylotermes is

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Fig. 13. Comparison of the ranges of maximum width of head, height of head, maximum width of labrum, maximum width of pronotum, length of hind femur, and length of hind tibia of the soldier caste among 45 Stylotermes species. Star, S. halumicus sp. nov.; asterisks, the Stylotermes species, with all its available measurements overlapped with those of S. halumicus; black squares, the range of measurements; gray squares, the range of measurements of S. halumicus.

challenged for taxonomic study. So far, many morphological vari- with morphological measurement and detail description would be ations were considered as interspecific variation by previous re- the first step to revise the genus. searchers, and hence numerous species were described. The boundary of intraspecific variation and interspecific variation Etymology would be difficult to be defined based on morphological data Stylotermes halumicus was found at the long-term study site of alone. The current study providing barcode gene sequences along Taiwanese pangolin (Manis pentadactyla pentadactyla L.) at

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Fig. 14. Living habitus and nest of Stylotermes halumicus. Soldiers, worker, and larva (A). Infesting tree, Zelkova serrata (Thunb.) Makino (arrow, the section of dead branch) (B). Infesting area (C). Gallery of S. halumicus (arrow, wet mud produced by termites) (D). Scale bar is 1 cm.

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