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

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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 halumi- cus 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. para- bengalensis 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. sinen- sis (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 spe- cies on the basis of numerous soldiers and workers from one col- ony 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 col- lected 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. 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 362 Annals of the Entomological Society of America, 2017, Vol. 110, No. 4 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).
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