A Review of the Colletes Succinctus-Group (Hymenoptera: Colletidae) from China with Redescription of the Male of C. Gigas

Zootaxa 3626 (1): 173–187 ISSN 1175-5326 (print edition) www.mapress.com/zootaxa/ Article ZOOTAXA Copyright © 2013 Magnolia Press ISSN 1175-5334 (online edition) http://dx.doi.org/10.11646/zootaxa.3626.1.7 http://zoobank.org/urn:lsid:zoobank.org:pub:B91163ED-773B-4FF7-8E6B-7B708CC8A894

A review of the Colletes succinctus-group (Hymenoptera: Colletidae) from China with redescription of the male of C. gigas

ZE-QING NIU1, MICHAEL KUHLMANN2 & CHAO-DONG ZHU1,3 1Key Laboratory of Zoological Systematics and Evolution (CAS), Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, P. R. China. E-mail: [email protected] 2Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom. . E-mail: [email protected] 3Corresponding author. E-mail: [email protected]

Abstract

Four species of the Colletes succinctus-group known from China are reviewed and a key to species is provided. Colletes gigas Cockerell, 1918 is recognized as a member of the Colletes succinctus-group for the first time based on a redescription of the male.

Key words: taxonomic review, bees, distribution

Introduction

The bee genus Colletes Latreille, 1802 is characterized by the outwardly arcuate posterior part of the second recurrent vein, the bilobate glossa and by the base of the propodeum that has a short subhorizontal to vertical basal zone, usually limited posteriorly by a carina or sharp change in slope or sculpture, and divided by longitudinal carina (Michener, 1989, 2007). Colletes currently includes 470 described species with an estimated total of about 700 species (Kuhlmann & Proshchalykin, 2011, Proshchalykin & Kuhlmann, 2012), from all continents except Antarctica, Australia, Madagascar and Southeast Asia (Michener, 2007). About 205 species are known from the Palearctic region with their centre of diversity in Middle Asia (Kazakhstan, Kyrgyzstan, Tajikistan, Turkmenistan, and Uzbekistan) (Kuhlmann, 2005, 2006, Proshchalykin & Kuhlmann, 2012). Within the genus Colletes, the C. succinctus-group (sensu Noskiewicz, 1936) is characterized by the putative synapomorphy of a pair of prominent, deep lateral groves on the male S6, the female can be recognized by apical margin of T1 medially without hair band, margin translucent yellow to orange, disc of T1 without hairs, and basal part of T1 laterally with dense patches of hairs. The group comprises fourteen described species in Palearctic region and divides into two subgroups: the collaris-subgroup with three species characterized by a very small oval- shaped male S7 and the succinctus-subgroup with eleven species and the males having a broad sickle-shaped S7 (Dubitzki & Kuhlmann 2004; Hölzler & Mazzucco, 2011, Kuhlmann, 2000, 2003). The collaris-subgroup has a trans-palearctic distribution with C. collaris Dours, 1872 known from Spain to Japan while C. bischoffi Noskiewicz, 1936 (Himalaya) and C. taiwanensis Dubitzky & Kuhlmann, 2004 (Taiwan) are restricted to the eastern Palearctic. Species of the succinctus-subgroup have their center of diversity in the western and central part of the Palearctic with C. reticulatus (Cameron, 1897) and C. bhutanicus Kuhlmann, 2003 (both Himalaya) on the southeastern edge of its distribution and C. arsenjevi Kuhlmann, 2006 in the eastern Palearctic (Kuhlmann & Quest, 2006). China is a country that stretches over a vast expanse of the Palearctic and Oriental region. Given its size as well as the geographical and climatic diversity and its direct neighborhood to one of the most important global centers of bee diversity in Middle Asia (Kuhlmann, 2005, 2006)), the Chinese Colletes fauna is estimated to comprise

Accepted by C. Rasmussen: 30 Jan. 2013; published: 12 Mar. 2013 173 100–150 species (Kuhlmann, unpublished), but the bee species of the genus are largely unexplored and nobody has ever dealt with these bees comprehensively in China. Currently little has been known about the Colletes fauna of the country; only 37 species have been recorded so far (Kuhlmann, 2000, 2002, 2007, 2009, unpublished records, Noskiewicz, 1936, Wu, 1965, 1982, 1987, 1992). From a review of the literature and examination of specimens at the Insect Collection of the Institute of Zoology, the Chinese Academy of Sciences (IZCAS), we recognized four Chinese species of the Colletes succinctus-group. For the iconic C. gigas Cockerell, 1918, the largest Colletes bee in the world, a redescription of the male is provided that for the first time allowed us to recognize this species as a member of the C. succinctus-group. An illustrated key to all four species of the C. succinctus-group known from China is provided and their distributions recorded.

Material and methods

All specimens examined are deposited in the Insect Collection of the IZCAS, Beijing, China. The specimens were examined with a NIKON SMZ 1500 stereomicroscope. Attributes were recorded with a NIKON D7000 digital camera. The terminology used in the redescription follows Michener (2007) for general morphology. Absolute measurements, in millimeters (mm), are used for length of body. For all other structures, relative measurements are used. Some abbreviations used in the redescription follows Niu et al. (2004, 2012) as follows: BL (body length): measured from the base of the antennal socket to the apex of the metasoma; HL (head length): measured from the apicomedian margin of the clypeus to the upper margin of the vertex in frontal view; HW (head width): measured at the widest point of the head across the compound eyes in frontal view; EW (eye width): the greatest width of eye in lateral view; GW (genal width): the greatest width of the gena in lateral view; MtW (metasomal width): measured at the widest metasomal tergum in dorsal view; TW (width between tegulae): the greatest width between out-margin of tegulae in dorsal view; T1, T2 etc. for first, second, etc. metasomal terga; S1, S2, etc. for first, second, etc. metasomal sterna; puncture density is expressed as the relationship between puncture diameter (d) and the space between them (i), such as i = 1.5d or i < d (Kuhlmann & Proshchalykin, 2011). Multiple specimens of C. collaris, C. luzhouensis Kuhlmann, C. clypearis Morawitz group and Hylaeus sp. (Table 1) were sequenced for DNA barcodes with the primers: 5’-TATCAACCAATCATAAAAATATTG-3’ and 5’- TAAACTTCTGGATGACCAAAAAATCA-3’ (Hastings et al., 2008). We compared our sequences with those deposited in the BOLD system (http://www.boldsystems.org). In addition we used MEGA 5 (Tamura et al., 2011) to reconstruct an NJ tree to confirm the positions and identities of some specimens with little morphological variance.

Results and discussion

Colletes Latreille, 1802

Key to the species of the Colletes succinctus-group known from China

1. Female (Flagellum 10 segmented) ...... 2 - Male (Flagellum 11 segmented) ...... 5 2. Body large and robust, body length 17–18 mm (Fig. 16), basal part of T1 with large lateral hair patches (Fig. 19) . . . C. gigas - Body small and slender, body length less than 15 mm (Figs. 1, 9), basal part of T1 with small lateral hair patches (Figs. 3, 11) ...... 3 3. Malar area distinctly longer than diameter of antennal flagellum ...... C. taiwanensis - Malar area nearly as long as diameter of antennal flagellum ...... 4 4. Apical hair band of T2 medially broad, punctation on disc of T1 dense (Fig. 3) ...... C. arsenjevi - Apical hair band of T2 medially narrow, punctation of disc of T1 more dispersed (Fig. 11) ...... C. collaris 5. Body large and robust, body length 13–17 mm (Fig. 19), T1–5 with broad apical hair bands (Fig. 22) ...... C. gigas - Body small, body length less than 12 mm (Figs. 4, 12, 19), T1–5 with narrow apical hair bands (Figs. 5, 15) ...... 6 6. Apical lobes of S7 large, sickle-shaped (Fig. 7) ...... C. arsenjevi - Apical lobes of S7 small, oval-shaped (Fig. 13) ...... 7 7. Apical margin of S7 convex ...... C. taiwanensis - Apical margin of S7 concave (Fig.13) ...... C. collaris

174 · Zootaxa 3626 (1) © 2013 Magnolia Press NIU ET AL. A REVIEW OF CHINESE COLLETES SUCCINCTUS-GROUP Zootaxa 3626 (1) © 2013 Magnolia Press · 175 176 · Zootaxa 3626 (1) © 2013 Magnolia Press NIU ET AL. A REVIEW OF CHINESE COLLETES SUCCINCTUS-GROUP Zootaxa 3626 (1) © 2013 Magnolia Press · 177 1. Colletes arsenjevi Kuhlmann, 2006 (Figs. 1–8)

Colletes arsenjevi Kuhlmann, 2006: 3 [Holotype: ♂, Russia, Primorskiy Terr., Lazovsky Nature Reserve, sandy coast (134°07'46"E, 43°01'07"N), 16–25. IX. 2001, Malaise trap, leg. M. Quest (IBSS)]; Proshchalykin, 2007b: 878; Quest, 2009: 119; Proshchalykin & Quest, 2009: 239; Kuhlmann, 2009: 18 [1♂, Jeminay County, Altay Prov., Xinjiang Uygur Aut. Reg., 27. VIII. 2002 (R. Murao); 2♀2♂, East of Jeminay, Altay Prov., Xinjiang Uygur Aut. Reg., 1300m, 28. VIII. 2002 (R. Murao, A. Dawut, O. Tadauchi)]; Kuhlmann & Proshchalykin, 2011: 20 [Distribution: China (Xinjiang)]. Colletes succinctus Osytshnjuk & Romankova, 1995: 483; Proshchalykin, 2003: 26; 2004: 3; Proshchalykin et al., 2004: 159.

Material examined. 2♀, China: Inner Mongolia, Tomortei (41°48'N, 113°06'E), 27. VIII. 1971, coll. no record; 6♀, China: Inner Mongolia, Tomortei (41°48'N, 113°06'E), 27. VIII. 1971, coll. no record; 4♀, China: Inner Mongolia, Hohhot (40°48'N, 111°42'E), 2. IX. 1989, coll. Huan-LI XU (Astragalus hungneensis); 1♀, China: Inner Mongolia, Hohhot (40°48'N, 111°42'E), 3. IX. 1989, coll. Huan-Li XU; 2♀, China: Inner Mongolia, Hohhot (40°48'N, 111°42'E), 4. IX. 1989, coll. Huan-Li XU; 1♀, China: Inner Mongolia, Xilin Gol Meng (43°48'N, 116°00'E), 22. VIII. 1971, coll. You-Wei ZHANG; 1♀, China: Gansu Prov., Jiuquan (39°42'N, 98°24'E), 1400m, 25. VIII. 1957, Coll. Yi-Ran ZHANG; 1♀, China: Shanxi, Taigu (37°24'N, 112°30'E), 16. IX. 1953, coll. no record; 1♀, China: Shanxi, Taigu (37°24'N, 112°30'E), 17. IX. 1953, coll. no record; 1♂, China: Inner Mongolia, Xilin Gol Meng (43°48'N, 116°00'E), 22. VIII. 1971, coll. You-Wei ZHANG; 1♂, China: Inner Mongolia, Xilin Gol Meng, Erenhot (43°36'N, 112°00'E), 23. VII. 1971, coll. no record; 1♂, China, Xinjiang, Jeminay, 47º22′N, 85º33′E, 1080m, 28. VIII. 2002, coll. Ze-Qing NIU; 3♂, China, Inner Mongolia, Dong Ujimqin, 45º30′N, 117º00′E, 19. VIII. 1971, coll. You-Wei ZHANG; 1♂, China, Inner Mongolia, Jarud Qi, Breeding Stock Field, 44º30′N, 120º54′E, 23. VIII. 1979, coll. Ju-Peng LIU. Floral association. Astragalus hungneensis (Fabaceae). Distribution in China. Xinjiang, Inner Mongolia, Gansu, Shanxi (Fig. 25). General distribution. Russia, Mongolia, China. Remark. In male C. arsenjevi, there is some minor variation in the length of the gonostylus among specimens collected at different sites (see Figs. 6, 8) which we consider to be within the range of variation of this species.

2. Colletes collaris Dours, 1872 (Figs. 9–15)

Colletes collaris Dours, 1872: 296, ♀, ♂ (type locality: “Cannes, Algére, îles de l’Archipel grec”); Noskiewicz, 1936: 485; Osytshnjuk, 1970: 76; Osytshnjuk & Romankova, 1995: 483; Proshchalykin, 2003: 26; 2004: 3; 2007a: 89; 2007b: 878; Proshchalykin et al., 2004: 158; Ignatenko, 2004: 109; Quest, 2009: 119; Proshchalykin & Quest, 2009: 239; Kuhlmann & Proshchalykin, 2011: 20 (Distribution: Western and North-eastern China); Proshchalykin & Kuhlmann, 2012: 8 (male, fig. f: S6). Colletes incerta Radoszkowski, 1891: 252, ♂ [type locality: “des environs de Vladivostok” (Primorskiy Terr., Russia)]. Colletes frigidus Pérez, 1903: 227–228, ♀, ♂ (type locality: SW France). Andrena riukiuensis Matsumura in Matsumura & Uchida, 1926: 69 (type locality: Japan, “Okinawa-honto”).

Material examined. 1♀, China: Beijing, Qinlongqiao (40°18'N, 116°00'E), 3. IX. 1988, coll. Huan-Li XU (Asteraceae); 5♀, China: Beijing, Qinlongqiao (40°18'N, 116°00'E), 5. IX. 1988, coll. Huan-Li XU (Asteraceae); 1♀, China: Beijing, Qinlongqiao (40°18'N, 116°00'E), 5. IX. 1988, coll. Huan-Li XU; 1♀, China: Beijing, Qinlongqiao (40°18'N, 116°00'E), 7. IX. 1982, coll. Zhu JI; 1♀, China: Beijing, Bada Ling (40°18'N, 116°00'E), 4. IX. 1986, coll. Jian-Guo FAN; 4♀, China: Beijing, Changping District, Liucun, Baiyanggou (40°14'N, 115°57'E), 6. IX. 2011, coll. Feng YUAN; 1♀, China: Beijing, Changxindian (39°48'N, 116°12'E), 5. IX. 1959, coll. no record; 1♀, China: Inner Mongolia, Alxa Zuoqi (38°48'N, 105°42'E), 18. IX. 1987, coll. Li-Zhu ZHANG; 1♀, China: Inner Mongolia, Xilin Gol Meng (43°48'N, 116°00'E), 16. VIII. 1979, coll. Ju-Peng LIU and Yong-Lin CHENG; 1♀, China: Heilongjiang, Da Hinggan Ling, Daxiangshu (51°42'N, 126°36'E), 18. VII. 1970, coll. no record; 1♀, China: Yunnan, Dêqên Xian, Adong (28°30'N, 98°54'E), 2700m, 9. V. 1981, coll. Shu-Yong WANG; 1♀, China: Yunnan, Zhongdian Xian (27°42'N, 99°42'E), 3250m, 22. VIII. 1981, coll. Shu-Yong WANG; 1♀, China: Yunnan, Dêqên Xian, (28°30'N, 98°54'E), 3300m, 2. IX. 1981, coll. Xue-Zhong ZHANG; 2♀, China:

178 · Zootaxa 3626 (1) © 2013 Magnolia Press NIU ET AL. FIGURES 1–8. Colletes arsenjevi Kuhlmann, 2006. 1, Female body in lateral view; 2, Female head in frontal view; 3, Female T1–2 in dorsal view, showing the punctures on disc of T1 and the pilosity on T1–2; 4, Male body in lateral view; 5, Male T1–2 in dorsal view, showing the punctures on disc of T1 and the pilosity on T1–2; 6, Male genitalia in lateral view, showing the gonostylus; 7, Male S7 in ventral view, showing the apical lobes; 8, Male genitalia in lateral view, showing variation of the gonostylus. Scale bar: 1mm.

A REVIEW OF CHINESE COLLETES SUCCINCTUS-GROUP Zootaxa 3626 (1) © 2013 Magnolia Press · 179 FIGURES 9–15. Colletes collaris Dours, 1872. 9, Female body in lateral view; 10, Female head in frontal view; 11, Female T1–2 in dorsal view, showing the punctures on disc of T1 and the pilosity on T1–2; 12, Male body in lateral view; 13, Male S7 in ventral view, showing the apical lobes; 14, Male genitalia in lateral view, showing the gonostylus; 15, Male T1–2 in dorsal view, showing the punctures on disc of T1 and the pilosity on T1–2. Scale bar: 1mm.

180 · Zootaxa 3626 (1) © 2013 Magnolia Press NIU ET AL. Yunnan, Zhongdian Xian, Daxueshan (24°06'N, 99°36'E), 4000m, 14. VIII. 1981, coll. Xue-Zhong ZHANG; 1♀, China: Yunnan, Dêqên, Baimangxueshandongpo (28°42'N, 98°54'E), 3300m, 28. VIII. 1981, coll. Xue-Zhong ZHANG; 2♀, China: Xizang, Linzhi Xian, Ecological Research Institute of Xizang Plateau (29°40'N, 94°21'E), 3000m, 23. VIII. 2008, coll. Zhao-Hui PAN; 5♀, China: Xizang, Linzhi Xian, Ecological Research Institute of Xizang Plateau (29°40'N, 94°21'E), 3000m, 10. IX. 2008, coll. Zhao-Hui PAN; 6♀, China: Xizang, Linzhi Xian, Ecological Research Institute of Xizang Plateau (29°40'N, 94°21'E), 3000m, 18. IX. 2008, coll. Zhao-Hui PAN; 3♀, China: Xizang, Linzhi Xian, Ecological Research Institute of Xizang Plateau (29°40'N, 94°21'E), 3000m, 13. X. 2008, coll. Zhao-Hui PAN; 4♀, China: Xizang, Linzhi Xian, Ecological Research Institute of Xizang Plateau (29°40'N, 94°21'E), 3000m, 20. X. 2008, coll. Zhao-Hui PAN; 1♀, China: Xizang, Linzhi Xian, Ecological Research Institute of Xizang Plateau (29°40'N, 94°21'E), 3000m, 27. X. 2008, coll. Zhao-Hui PAN; 1♂, China: Beijing, Qinlongqiao (40°18'N, 116°00'E), 3. IX. 1988, coll. Huan-Li XU (Asteraceae); 1♂, China: Beijing, Qinlongqiao (40°18'N, 116°00'E), 5. IX. 1988, coll. Huan-Li XU (Asteraceae); 1♂, China: Beijing, Bada Ling (40°18'N, 116°00'E), 15. IX. 1977, coll. Shu-Fang WANG (Asteraceae); 1♂, China: Beijing, Bada Ling (40°18'N, 116°00'E), 15. IX. 1977, coll. Shu-Fang WANG; 1♂, China: Hebei, Wuling Shan (40°24'N, 117°24'E), VIII. 1974, coll. no record; 1♂, China: Sichuan Prov., Barkam (31°54'N, 102°12'E), 2900m, 22. VIII. 1983, coll. Rui-Qi WANG; 1♂, China: Sichuan, Wenchuan, Yingxiu (31°00'N, 103°30'E), 16. IX. 1983, coll. Xue-Zhong ZHANG; 2♂, China: Sichuan, Batang, Yidun (30°18'N, 99°18'E), 3470m, 16. VIII. 1982, coll. Shu-Yong WANG; 1♂, China: Sichuan, Yajiang (30°00'N, 101°00'E), 3300m, 25. VII. 1982, coll. Xue-Zhong ZHANG; 1♂, China: Xizang, Bomi (29°48'N, 95°42'E), 700m, 2–3. IX. 1983, coll. Yin-Heng HAN; 3♂, China: Xizang, Mainling, Jiage (29°12'N, 94°06'E), 3000m, 20. IX. 1974, coll. Fu-Sheng HUANG; 1♂, China: Yunnan, Xiaozhongdian (27°30'N, 99°48'E), 3200m, 2. VIII. 1982, coll. Jian-Guo FAN; 1♂, China: Yunnan, Xiaozhongdian (27°30'N, 99°48'E), 3200m, 2. VIII. 1984, coll. Shu-Yong WANG; 1♂, China: Yunnan, Lanping (26°24'N, 99°12'E), 2400m, 27. VIII. 1984, coll. Rui-Qi WANG; 1♂, China: Yunnan, Lanping (26°24'N, 99°12'E), 2350m, 25. VIII. 1984, coll. Jian-Guo FAN; 1♂, China: Yunnan, Dêqên (28°40'N, 98°54'E), 3300m, 28. VIII. 1981, coll. Xue-Zhong ZHANG; 2♂, China: Beijing, Changping District, Liucun, Baiyanggou (40°14'N, 115°57'E), 6. IX. 2011, coll. Feng YUAN; 1♂, China: Beijing, Miaofeng Shan (40°00'N, 116°00'E), 30. IX. 1957, coll. Min-Hui WANG; 1♂, China: Inner Mongolia, Xilin Gol Meng (43°48'N, 116°00'E), 18. IX. 1979, coll. Yon-Lin CHEN; 1♂, China: Inner Mongolia, Dong Ujimqin (45°30'N, 117°00'E), 18. IX. 1971, coll. You-Wei ZHANG; 1♂, China: Inner Mongolia, Xilin Gol Meng (43°48'N, 116°00'E), 22. VII. 1971, coll. You-Wei ZHANG; 1♂, China: Heilongjiang, Mishan (45°30'N, 131°48'E), 12. VIII. 1970, coll. no record; 1♂, China: Heilongjiang, Yichun Wuyiling (48°30'N, 129°24'E), 28. VIII. 1970, coll. Zhi-Xiang CHENG; 1♂, China: Beijing, Bada Ling (40°18'N, 116°00'E), 8. IX. 1980, coll. Shu- Fang WANG; 1♂, China: Sichuan, Wan Xian (30°48'N, 108°18'E), 1200m, 29. IX. 1994, coll. Jun CHEN; 1♂, China: Qinghai, Yushu Xian (33°00'N, 99°00'E), 3700m, 26. VIII. 1964, coll. Shu-Yong WANG; 1♂, China: Yunnan, Lanping Xian (26°24'N, 99°12'E), 2350m, 24. VIII. 1984, coll. Jian-Guo FAN; 1♂, China: Yunnan, Lanping Xian (26°24'N, 99°12'E), 2350m, 22. VIII. 1984, coll. Jian-Guo FAN; 1♂, China: Yunnan, Zhongdian Xian, Daxueshan (24°06'N, 99°36'E), 4000m, 14. VIII. 1981, coll. Xue-Zhong ZHANG; 5♂, China: Xizang, Linzhi Xian, Beach of Niyang River (29°38'N, 94°22'E), 2985m, 26. VIII. 2012, coll. Ze-Qing NIU (Tamarix chinensis); 4♂, China: Xizang, Linzhi Xian, Beach of Niyang River (29°40'N, 94°21'E), 2990m, 27. VIII. 2012, coll. Ze-Qing NIU (Tamarix chinensis); 2♂, China: Xizang, Linzhi Xian, Ecological Research Institute of Xizang Plateau (29°40'N, 94°21'E), 3000m, 10. IX. 2008, coll. Zhao-Hui PAN; 3♂, China: Xizang, Linzhi Xian, Ecological Research Institute of Xizang Plateau (29°40'N, 94°21'E), 3000m, 18. IX. 2008, coll. Zhao-Hui PAN; 1♂, China: Xizang, Linzhi Xian, Ecological Research Institute of Xizang Plateau (29°40'N, 94°21'E), 3000m, 13. X. 2009, coll. Zhao-Hui PAN; 1♂, China: Xizang, Mainling Xian, Lanyigou (29°12'N, 94°06'E), 2960m, 22. IX. 2008, coll. Zhao-Hui PAN; 1♂, China: Jiangxi, Guling (29°30'N, 115°54'E), 13. IX. 1934, coll. O. PIEL; 1♂, China: Heilongjiang, Tongjiang (47°36'N, 132°30'E), 11. VIII. 1970, coll. no record; 1♂, China: Heilongjiang, Harbin (45°42'N, 126°36'E), 11. VIII. 1970, coll. no record. Floral association. Asteraceae; Tamarix chinensis (Tamaricaceae). Distribution in China. Beijing, Sichuan, Xizang, Yunnan, Inner Mongolia, Heilongjiang (Fig. 25). General distribution. Spain, France, Germany, Switzerland, Austria, Italy, Czech Republic, Hungary, Russia, Kazakhstan, Mongolia, South Korea, Japan, China. Remark. Colletes collaris females are known to be broadly oligolectic on Asteraceae pollen (Müller & Kuhlmann, 2008). Males are flexible flower visitors for nectar and all specimens recently collected in Xizang

A REVIEW OF CHINESE COLLETES SUCCINCTUS-GROUP Zootaxa 3626 (1) © 2013 Magnolia Press · 181 (Linzhi Xian, bank of Niyang River) were exclusively found on Tamarix chinensis. Males from Xizang, Sichuan and Yunnan show a high degree of morphological variation particularly in the shape of S7. This is unusual for C. collaris where morphological variation is almost lacking in specimens found from Spain to NE China. However, DNA barcoding of specimens from distantly located Xizang and Beijing (Table 1) show no significant difference among the specimens (Fig. 24), thus suggesting that they are conspecific. However, Kuhlmann et al. (2007) found lack of genetic differences for the COI in three morphologically very similar but biologically (flower preferences) and phenologically well defined Colletes species in western Europe, that also belong to the C. succinctus-group. The subtle morphological differences between them are diagnostic and fall within the range observed in specimens of C. collaris from southern China suggesting the potential existence of cryptic species. However, due to the lack of fresh material suitable for barcoding from Sichuan and Yunnan and the limited number of specimens available for morphological studies for the moment we here assume that they all represent a single species C. collaris. A more extensive study based on additional freshly collected material from various parts of southern China including biological observations (flower preferences, phenology, habitat requirements) is needed to clarify the taxonomic situation.

3. Colletes gigas Cockerell, 1918 (Figs. 16–23)

Colletes gigas Cockerell, 1918: 158–159, ♀ [type locality: China: Foochow, Fukien, 16. IV. 1914 (C. R. Kellogg, 243), from Prof. C. R. Baker]; Wu, 1965: 28, ♀♂; Kuhlmann, 1999: 77; Yasumatus, 1936: 244, ♂; Zhao et al., 2010: 1287 (Nesting Biology).

Redescription. Male, body large, BL: 13–17mm (Fig. 19); head broader than long (Fig. 20), HW: HL=89:73; gena slightly narrower than eye, GW: EW =18: 21; width of metasoma nearly as wide as that between tegulae, MtW: TW=102: 101. Facial fovea narrow, nearly as wide as antennal flagellum; clypeus longer than broad, with longitudinal and deep sculptures, apex with a pair of deep lateral grooves, surface between sculpture smooth and shiny; vertex behind eyes rounded; vertex and genae with round and dense punctures, d=3–4i; supraclypeal area and paraocular area with large and dense oblique needled punctures, d=5–6i; malar area broader than long, medially about as long as 1/2 width of mandible base; mesoscutum and scutellum with large and round punctures, size of punctures larger than that of vertex, d=3–4i; disc of T1 with round punctures, size of punctures less than that of mesoscutum, d=1–2i (Fig. 22); antenna short, extending to the apex of scutellum, first flagellomere slightly broader than long, half as long as second flagellomere, flagellomeres 2–11 roughly twice as long as broad and nearly equal to each other in length; mandible with preapical tooth on upper margin; stigma of fore wings broader than prestigma, but nearly equal in length, jugal lobe of hind wings large, nearly five-sixth as long as ventral lobe; hind basitarsi normal, not broadened; S6 with a pair of deep lateral grooves at apex; genitalia in lateral view as in Fig. 23, gonostylus lengthened triangular with sparse long hairs; S7 with broaden sickle-shaped haired apical lobes (Fig. 21, in ventral view). Clypeus, mandible, vertex, frons, antenna, pronotal lobe, mesoscutum, scutellum and all legs black except tips of mandible partly dark reddish-brown. Wings hyaline; wing venations dark brown. Metasomal terga black except narrow apical margins brownish translucent. Pubescence dense; face (Fig. 20), gena, pronotal lobe, mesepisternum, scutellum and surface of propodeum with long yellow plumose hairs, vertex, and mesoscutum with long yellow plumose hairs, entraining some blackish plumose hairs; sloping anterior part and lateral part of T1 densely covered erect long yellow plumose hairs, disc of T1 sparsely covered with long and erect yellow plumose hairs; disc of T2–T6 covered sparse blackish brown hairs; T1–T5 with broad yellowish white apical tergal hair bands, T2 with broad yellowish brown basal tergal hair band, and the basal tergal hair band often hidden by T1 in smaller specimens; S5 without distinctly longer hairs medially, only with longer hairs laterally; coxae, trochanteres, and femora of all legs with plumose yellow hairs, forming scopa. Material examined. 4♀, China: Guizhou, Huaxi (26°24'N, 106°42'E), 12. X. 1983, coll. Jian-Guo Fan (Camellia oleifera); 3♀, China: Guizhou, Huaxi (26°24'N, 106°42'E), 11. X. 1983, coll. Jian-Guo Fan (Camellia oleifera); 5♀, China: Zhejiang, Anji (30°36'N, 119°36'E), date and coll. no record (Camellia oleifera); 1♀, China, Zhejiang, Hangzhou (30°12'N, 120°06'E), 1934, coll. no record; 1♀, China, Zhejiang, Hangzhou (30°12'N, 120°06'E), 1933, coll. no record; 1♀, China, Zhejiang, Hangzhou (30°12'N, 120°06'E), 26. XI. 1934, coll. no record; 1♀, China, Zhejiang, Hangzhou (30°12'N, 120°06'E), 24. IX. 1932, coll. no record; 1♀, China, Zhejiang,

182 · Zootaxa 3626 (1) © 2013 Magnolia Press NIU ET AL. FIGURES 16–23. Colletes gigas Cockerell, 1918. 16, Female body in lateral view; 17, Female head in frontal view; 18, Female T1–2 in dorsal view, showing the punctures on disc of T1 and the pilosity on T1–2; 19, Male body in lateral view; 20, Male head in frontal view; 21, Male S7 in ventral view, showing the apical lobes; 22, Male T1–2 in dorsal view, showing the punctures on disc of T1 and the pilosity on T1–2; 23, Male genitalia in lateral view, showing the gonostylus. Scale bar: 1mm.

A REVIEW OF CHINESE COLLETES SUCCINCTUS-GROUP Zootaxa 3626 (1) © 2013 Magnolia Press · 183 Wenzhou (28°00'N, 120°36'E), 15. V. 1928, coll. no record; 2♀, China: Fujian, Tiankui (24°30'N, 118°48'E), 5. XI. 1980, coll. Ron-Quan CAI; 2♀, China: Fujian, Baihua Hills (26°06'N, 119°18'E), 14. XII. 1914, coll. Y.M.; 1♀, China: Guangdong, Dinghu Mountain (23°06'N, 112°30'E), date and coll. no record; 4♂, China: Guizhou, Huaxi (26°24'N, 106°42'E), 12. X. 1983, coll. Jian-Guo Fan (Camellia oleifera); 4♂, China: Guizhou, Huaxi (26°24'N, 106°42'E), 11. X. 1983, coll. Jian-Guo Fan (Camellia oleifera); 4♂, China: Zhejiang, Anji (30°36'N, 119°36'E), 1972, coll. no record (Camellia oleifera); 1♂, China: Zhejiang, Hangzhou (30°12'N, 120°06'E), 3. III. 1935, coll. no record; 1♂, China: Hunan, Changsha (28°12'N, 112°54'E), XII. 2008, coll. Liang DING. Floral association. Camellia oleifera (Theaceae). Distribution in China. Fujian, Guangdong, Zhejiang, Guizhou, Hunan (Fig. 25). General distribution. China. Remark. Kuhlmann (1999: 77) mentioned that “Noskiewicz (1936: 293) did not study the species but suspected that C. gigas is related to C. lacunatus Dours. The male was described by Yasumatsu in 1936, but most of the text is in Chinese and he failed to describe the genitalia and the 7th ventral plate, that are among the most important characters”. Here the male is redescribed and examination of S6 (with a pair of apicolateral grooves) and the shape of S7 clearly show that C. gigas belongs to the C. succinctus-group.

4. Colletes taiwanensis Dubitzky & Kuhlmann, 2004

Colletes taiwanensis Dubitzky & Kuhlmann, 2004: 272–278, ♀♂ (type locality: China, Taiwan, Yuanfeng, 2800m, 24°07'N, 121°14'E, 12. IX. 2002, leg. A. Dubitzky & S. Szczepanek.) Holotype: ♀ (NCHUT), Central Taiwan (ROC), Yuanfeng (2800m), 24°07'N, 121°14'E, floral record: Senecio nemorensis, 12. IX. 2002, leg. A. Dubitzky & S. Szczepanek. Paratypes: 2♀ (CDS), same data as holotype; 1♀ (CDS), Central Taiwan (ROC), entrance Taroko National-Park (3100 m), 24°07'N, 121°16'E, floral record: Senecio nemorensis, 12. IX. 2002, leg. A. Dubitzky & S. Szczepanek; 1♀ (TARI), Central Taiwan (ROC), Sungkang (2100m), Nantou Hsien, Malaise trap X. 1984, leg. K.S. Lin & K.C. Chou; 2♂ (NCHUT, CDS), Central Taiwan (ROC), Yuanfeng (2800 m), 24°07'N, 121°14'E, floral record: Senecio nemorensis, 11. IX. 2002, leg. A. Dubitzky & S. Szczepanek; 1♂ (CDS), Taiwan (ROC), Tengchih (1800m), 23°04'N, 120°48'E, floral record: Bidens alba, 18. IX. 2002, leg. A. Dubitzky & S. Szczepanek. 2♂, 3♀ (TARI, ZSM), Central Taiwan (ROC), Tayuling (2560 m), Hualien Hsien, 12.–15. IX. 1980, leg. K.S. Lin & C.H. Wang; 1♂ (TARI), Central Taiwan (ROC), Meifeng (2150 m), Nantou Hsien, Malaise trap, X. 1985, leg. K.S. Lin; 5♂, 1♀ (NMNS, ZSM, 1♂ CK), Taiwan, Kaoshiung, Yushan National Park, 24.–28. X. 1990, leg. C.K. Starr & S.S. Lu; 1♂ (NMNS), Taiwan, Kaoshiung, Yushan National Park, yellow pan trap, 24.–28. X. 1990, leg. C.K. Starr.

Material examined. None examined. Floral association. Senecio nemorensis (Asteraceae), Bidens alba (Asteraceae). Distribution in China. Taiwan (Fig. 25). General distribution. China.

Acknowledgements

The authors wish to thank Dr. Claus Rasmussen, Prof. Yan-Ru WU, Dr. Yan-Zhou Zhang, Dr. F. Javier Oritz- Sánchez and two anonymous reviewers for their comments and suggestions on the earlier drafts of the manuscript. Dr. Douglas Chesters checked the English language of parts of the manuscript. Qing-Yan DAI sequenced DNA barcodes and helped to reconstruct the phylogenetic trees. Da-Sheng WANG, Zhao-Hui PAN, Huan-Xi CAO and Qing-Tao WU contributed a lot in the field trip to the Southeast Tibet for collecting C. collaris. We also appreciate all previous collectors who made the rich collection of Colletes in IZCAS for our study. This work was supported mainly by grants from the National Science Foundation, China (Grants Nos. 31272264, J0930004) to Ze-Qing NIU, the Knowledge Innovation Program of the Chinese Academy of Sciences (Grant No. KSXC2-EW-B-02), and the National Science Foundation, China (Grants Nos. 30870268, 31172048, J1210002) to Chao-Dong ZHU.

184 · Zootaxa 3626 (1) © 2013 Magnolia Press NIU ET AL. FIGURES 24. NJ tree based on sequenced DNA barcode of the mitochondrial COI from different specimens of C. collaris. For details of the sequenced specimens see Table 1.

A REVIEW OF CHINESE COLLETES SUCCINCTUS-GROUP Zootaxa 3626 (1) © 2013 Magnolia Press · 185 FIGURE 25. Records of species of the Colletes succinctus-group in China. ●: Colletes arsenjevi Kuhlmann, 2006; ▲: Colletes collaris Dours, 1872; ʦ : Colletes gigas Cockerell, 1918; ɷ : Colletes taiwanensis Dubitzky & Kuhlmann, 2004.

References cited

Cockerell, T.D.A. (1918) Descriptions and records of bees. – LXXIX. Annals and Magazine of Natural History, Ser. 9, 1, 158–167. http://dx.doi.org/10.1080/00222931808562297 Dours, J.A. (1872) Hyménoptères nouveaux du bassin mediterranéen. Revue et Magasin de Zoologie, 23, 293–311, 349–359, 396–399, 419–434. Dubitzky, A. & Kuhlmann, M. (2004) First record of the bee genus Colletes for Taiwan with description of a new species (Hymenoptera, Apoidea, Colletidae). Deutsche Entomologische Zeitschrift, 51, 271–278. http://dx.doi.org/10.1002/mmnd.20040510209 Hastings, J. M., Schultheis, P. J., et al. (2008). DNA barcoding of new world cicada killers (Hymenoptera : Crabronidae). Zootaxa, 1713, 27–38. Hölzler, G. & Mazzucco, K. (2011) Preliminary description of Colletes pannonicus nov.sp., a member of the Colletes succinctus group, from eastern Austria (Insecta: Hymenoptera: Colletidae). Entomofauna, 32, 273–276. Ignatenko, E.V. (2004) The fauna and biology of bees of the family Colletidae (Hymenoptera, Apoidea) in Amur Province. A.I. Kurentsov's Annual Memorial Meetings, 15, 108–115. Kuhlmann, M. (1999) Colletes wolfi spec, nova from Italy, and Lectotype designation for Palearctic Bees of the Genus Colletes LATR., with Notes on new Homonymies and Synonymies (Hymenoptera: Apidae: Colletinae). Linzer biologische Beiträge, 31, 71–81. Kuhlmann, M. (2000) Katalog der paläarktischen Arten der Bienengattung Colletes LATR., mit Lectotypenfestlegungen, neuer Synonymie und der Beschreibung von zwei neuen Arten (Hymenoptera: Apidae: Colletinae). Linzer biologische Beiträge, 32(1), 155–193. Kuhlmann, M. (2002) Neue Arten der Bienengattung Colletes Latr. aus Südtibet mit Beschreibung der Route der “Deutschen Tibet Expedition Ernst Schäfer 1938/39” (Hymenoptera: Apidae: Colletinae). Linzer biologische Beiträge, 34, 1155–1178. Kuhlmann, M. (2003) Zur Kenntnis paläarktischer Bienen der Gattung Colletes Latr. Mit Beschreibung neuer Arten (Hymenoptera: Apidae: Colletinae). Linzer biologische Beiträge, 35, 723–746. Kuhlmann, M. (2005) Faunistik und Zoogeographie der Bienengattung Colletes Latreille 1802 (Hymenoptera: Apidae: Colletinae) in Mittelasien. Linzer biologische Beiträge, 37, 1353–1396.

186 · Zootaxa 3626 (1) © 2013 Magnolia Press NIU ET AL. Kuhlmann, M. (2006) Zur Biogeographie der Seidenbienen (Hymenoptera: Colletidae: Colletes Latr.) im Bienen- Diversitätszentrum Mittelasiens. Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie, 15, 89–92. Kuhlmann, M. (2007) Neue Colletes-Arten aus China mit Anmerkungen zu weiteren Arten (Hymenoptera: Apoidea: Colletidae). Linzer biologische Beiträge, 39, 463–474. Kuhlmann, M. (2009) Bees of the Genus Colletes (Hymenoptera, Colletidae) from Central Asia Collected by the Kyushu University Expeditions. ESAKIA, 49, 15–20. Kuhlmann, M., Else, G.R., Dawson, A. & Quicke, D.L.J. (2007) Molecular, biogeographical and phenological evidence for the existence of three western European sibling species in the Colletes succinctus group (Hymenoptera: Apidae). Organisms, Diversity and Evolution, 7, 155–165. http://dx.doi.org/10.1016/j.ode.2006.04.001 Kuhlmann, M. & Proshchalykin, M. Y. (2011) Bees of the genus Colletes Latreille 1802 of the Asian part of Russia, with keys to species (Hymenoptera: Apoidea: Colletidae). Zootaxa, 3068, 1–48. Kuhlmann, M. & Quest, M. (2006) A new species of the bee genus Colletes Latreille, 1802 (Hymenoptera: Colletidae) from the Russian Far East and Mongolia. Far Eastern entomologist, 157, 1–4. Matsumura, S. & Uchida, T. (1926) Die Hymenopteren-Fauna von den Riukiu-Inseln. Insecta Matsumurana, 1(1), 32–52, 1(2) 63–77 + pl. 3. Michener, C.D. (1989) Classification of American Colletinae (Hymenoptera, Apoidea). University of Kansas Science Bulletin, 53, 622–703. Michener, C.D. (2007) The Bees of the World. 2nd Edition. The Johns Hopkins University Press, Baltimore, 992 pp. Müller A. & Kuhlmann M. 2008. Pollen hosts of western palaearctic bees of the genus Colletes (Hymenoptera: Colletidae): the Asteraceae paradox. Biological Journal of the Linnean Society, 95, 719–733. http://dx.doi.org/10.1111/j.1095-8312.2008.01113.x Niu, Z.Q., Wu, Y.R. & Huang, D.W. (2004) A Taxonomic Study on the Subgenus Seladonia (Hymenoptera, Halictidae, Halictus) in China with Description of One New Species. Zoological Studies, 43(4), 647–670. Niu, Z.Q., Wu, Y.R. & Zhu, C.D. (2012) A new species of Bathanthidium Mavromoustakis (Hymenoptera: Megachilidae: Anthidiini) from China, with a key to the species. Zootaxa, 3218, 59–68. Noskiewicz, J. (1936) Palearktyczne gatunki rodzaju Colletes [Die palearktischen Colletes-Arten]. Prace Naukowe. Wydawnictwo Towarzystwa Naukowego we Lwowie, [2]3, 1–532, tab. i–xxviii. Osytshnjuk, A. Z. (1970) Fauna of the Ukraine. Vol. 12. Bees [Apoidea]. No. 4. Family Colletidae. Naukova Dumka, Kiev, 158pp. Osytshnjuk A.S. & Romankova T.G. (1995) Colletidae. In: Lehr P.A. (Ed.) Key to the insects of Russian Far East in six volumes. Vol. IV. Neuropteroidea, Mecoptera, Hymenoptera. Part 1. Nauka, St. Petersburg, pp. 480–489. Pérez, J. (1903) Espéces nouvelles de melliféres. Actes de la Société Linnéenne de Bordeaux, 58, 78–93, 208–236. Proshchalykin, M.Yu. (2003) Bee fauna (Hymenoptera, Apoidea) of Middle and Lower Amur region. Euroasian Entomological Journal, 2(1), 2–529. Proshchalykin, M.Yu. (2004) A check list of the bees (Hymenoptera, Apoidea) of the southern part of the Russian Far East. Far Eastern entomologist, 143, 1–17. Proshchalykin, M.Yu. (2007a) The fauna of bees (Hymenoptera, Apoidea) of the Jewish Autonomous Region. A.I. Kurentsov's Annual Memorial Meetings, 18, 88–93. Proshchalykin, M.Yu. (2007b) Fam. Colletidae. In: Lelej, A.S. (Ed.). Key to the insects of Russian Far East. Vol. 4. Pt 5. Dalnauka, Vladivostok, 878–883. Proshchalykin, M.Yu. & Kuhlmann, M. (2012) The bees of the genus Colletes Latreille 1802 of the Ukraine, with a key to species (Hymenoptera: Apoidea: Colletidae). Zootaxa, 3488, 1–40. Proshchalykin, M.Yu., Lelej, A.S. & Kupianskaya, A.N. (2004) Bee fauna (Hymenoptera, Apoidea) of Sakhalin Island. In: B o gato v, V. V. ( Ed .) . Flora and Fauna of Sakhalin Island (Materials of International Sakhalin Island Project). Part 2. Dalnauka, Vladivostok, 154–192. Proshchalykin, M.Yu. & Quest, M. (2009) Section Apiformes – Bees. In: Storozhenko, S.Yu. (Ed.). Insects of Lazovsky Nature Reserve. Dalnauka, Vladivostok, 238–250. Quest, M. (2009) Artbestand, Ökologie und Habititatwahl von Bienen ausgewählter Offenlebensräume im Lazovski Zapovednik (Ferner Osten Russland) (Hymenoptera, Apiformes). Entomofauna, 15(Suppl.), 1–357. Radoszkowski, O. (1891) Révision des armatures copulatrices des males du genre Colletes. Horae Societatis Entomologicae Rossicae, 25, 249–260. Tamura, K., Peterson, D., Peterson, N., et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution, 28, 2731–2739. http://dx.doi.org/10.1093/molbev/msr121 Wu Y.R. (1965) Economic Insect Fauna of China. Fasc. 9, Hymenoptera: Apoidea. Science Press, Beijing, 83pp. Wu Y.R. (1982) Hymenoptera: Apoidea. In: Huang, F.S. (Ed.), Insects of Xizang Vol. II. Science Press, Beijing, pp. 379–426. Wu Y.R. (1987) Hymenoptera: Apoidea. In: Zhang, S.M. (Ed.), Agricultural Insects, Spiders, Plant Diseases and Weeds of Xizang Vol. II. Xizang People’s Press, Lasa, pp. 237–245. Wu Y.R. (1992) Hymenoptera: Apoidea. In: Cheng S.X. (Ed.), Insects of the Hengduan Mountains Region Vol. II. Science Press, Beijing, pp. 1378–1421. Yasumatsu, K. (1936) A list of the known species of Colletidae from China and Japan, with description of the male of Colletes gigas Ckll. (Hym.). Entomology and Phytopathology, 4, 241–246. Zhao Y.H., Ding L., Yuan F., Zhang Y.Z., Tu, L.H. and Zhu, C.D. (2010) Nesting biology of Colletes gigas Cockerell (Hymenoptera: Colletidae). Acta Entomologica Sinica, 53, 1287–1294.