bees of the colletes flavicornis-group from china with description of one new species (hymenoptera:...

ZOOTAXA

ISSN 1175-5326 (print edition)

ISSN 1175-5334 (online edition)Copyright © 2014 Magnolia Press

Zootaxa 3780 (3): 534–546

www.mapress.com/zootaxa/Article

http://dx.doi.org/10.11646/zootaxa.3780.3.5

http://zoobank.org/urn:lsid:zoobank.org:pub:746D9B56-CA06-4849-BBF9-3847A2F80F5E

Bees of the Colletes flavicornis-group from China with description of one new

species (Hymenoptera: Apoidea: Colletidae)

ZE-QING NIU1, CHAO-DONG ZHU1,3 & MICHAEL KUHLMANN2,3

1Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road,

Chaoyang District, Beijing, 100101, P. R. China. E-mail: [email protected] of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom.3Corresponding author. E-mail: [email protected]; [email protected]

Abstract

Two species of the Colletes flavicornis-group from China are treated in this paper. C. vestitus sp. n. from Xinjiang is il-

lustrated and described, and C. popovi Noskiewicz, 1936 is illustrated and redescribed. Both sexes of the two species are

in addition characterized by DNA barcodes. The type specimens of the new species are deposited in the Insect Collection

of Institute of Zoology, Chinese Academy of Sciences, Beijing, China.

Key words: Apiformes, taxonomy, DNA barcode, fauna

Introduction

The Colletes flavicornis-group comprises nine described species (Table 1) from the Palaearctic Region (Kuhlmann

& Proshchalykin 2013a, b). Species of this group are mainly distributed in Central Asia (Kuhlmann 2005, 2006;

Kuhlmann & Proshchalykin 2013a), only C. emaceatus Noskiewicz, 1936, C. gusi Kuhlmann, 2009, C.

plumuloides Kuhlmann & Proshchalykin, 2013 and C. popovi Noskiewicz, 1936 occur outside this area (Kuhlmann

& Dorn 2002; Kuhlmann 2009; Kuhlmann & Proshchalykin 2013b) with C. popovi being the only species of this

group previously recorded from China (Noskiewicz 1936). In the species of C. flavicornis-group, the disc of the

mesonotum is smooth or sparsely and finely punctate, intervals much wider than the diameter of punctation.

Antennal flagella are ventrally brownish red to yellowish brown. The clypeus is elongate, as long as wide or longer,

and apically sparsely punctate. Malar area of females is slightly and of males distinctly elongate, being much

longer than half of the width of the base of mandible (Noskiewicz 1936). Based on recently collected specimens

and from a review of published information, we here record two species of the C. flavicornis-group from China

with C. vestitus sp. n. described as new. To facilitate their identification, both C. vestitus sp. n. and C. popovi are

illustrated, described. As there are few morphological features to group males and females of the same species in

this species group, we sequenced both sexes for DNA barcoding to confirm their species identities.

Material and methods

All specimens examined are deposited in the Insect Collection of Institute of Zoology, Chinese Academy of

Sciences (IZCAS), Beijing, China. The specimens were examined with a NIKON SMZ 1500 stereomicroscope.

Attributes were recorded with a NIKON D7000 digital camera and stacked with Helicon Focus software. 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. (2013) 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

534 Accepted by C. Rasmussen: 21 Feb. 2014; published: 24 Mar. 2014

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; punctation density is expressed as the relationship between punctation diameter (d) and the space between

them (i), such as i = 1.5d or i < d.

Multiple specimens of Colletes collected from China (Table 2) 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 a NJ tree to confirm the

positions and identities of some specimens with little morphological variance (Fig. 5).

Taxonomy

A checklist of the species of the Colletes flavicornis-group is shown in Table 1.

TABLE 1. Checklist of the species of the Colletes flavicornis-group. Distribution based on Kuhlmann & Proshchalykin

(2013a, b).

Colletes popovi Noskiewicz, 1936

(Figs 1a–f, male; 2a–f, female; 6)

Colletes popovi Noskiewicz, 1936: 271–274, ♀, ♂ [Lectotype: ♂, designated by Kuhlmann 2000: 172: Schibendu Schigusa s. Satschjou, Gasch. Gob., 9–12.VIII.[18]95, Rob[orovsky] and Kozlov (Zoological Institute, St.Petersburg, Russia)].

Redescription. Male, BL=6.5–7.0mm (Fig 1a); head broader than long (Fig 1b), HW:HL=46:35; gena narrower

than eye in lateral view, GW:EW=6:9; width of metasoma slightly narrower than that between tegulae,

MtW:TW=38:43. Antenna short, extending to scutellum, first flagellomere nearly as long as broad, 0.9 times as

long as second flagellomere, second flagellomere longer than broad, nearly 1.3 times as long as broad,

flagellomeres 3–11 roughly 1.4 times as long as broad and nearly equal to each other in length (Fig 1b); malar area

medially about 3/4 long as width of mandible base; facial fovea narrow, only 0.5 times as wide as antennal

flagellum; propodeum laterally covered with sparse long erect hairs, integumental sculpture completely visible;

disc of scutum and scutellum smooth and shiny, without punctation; posterior margin of T1 dark brown; disc of T1

dispersed and finely punctate, i=1.0–2.0d; T1–T5 with white apical hair bands, the band on T1 uninterrupted and

Species Female Male sp. n. Distribution

C. alicularis Noskiewicz, 1936 √ √ Turkmenistan, Kazakhstan, Tajikistan

C. emaceatus Noskiewicz, 1936 √ √ Turkmenistan, Kazakhstan, Mongolia

C. flavicornis Morawitz, 1876 √ √ Turkmenistan, Kazakhstan, Uzbekistan, Tajikistan

C. gusi Kuhlmann, 2009 √ √ Mongolia

C. kaline Kuhlmann & Proshchalykin, 2013 √ Turkmenistan

C. pallipes Noskiewicz, 1936 √ Kazakhstan

C. plumuloides Kuhlmann & Proshchalykin, 2013 √ Mongolia

C. plumulosus Noskiewicz, 1936 √ √ Kazakhstan, Uzbekistan

C. popovi Noskiewicz, 1936 √ √ Kazakhstan, Mongolia, China

C. vestitus sp. n. √ √ √ China

Total 9 8 1

Zootaxa 3780 (3) © 2014 Magnolia Press · 535COLLETES FLAVICORNIS-GROUP FROM CHINA

FIGURE 1. Colletes popovi Noskiewicz, 1936, male. a: Body in lateral view; b: Head in frontal view; c: Metasoma in dorsal view, showing T1–T2; d: S7 in dorsal view; e: Genitalia in lateral view; f: Genitalia in dorsal view. Scale bar: a, b, c, 1mm; d, e, f, 0.5mm.


FIGURE 2. Colletes popovi Noskiewicz, 1936, female. a: Body in lateral view; b; Head in frontal view; c: Head in lateral view; d: Mesonotum in dorsal view; e: Metasoma in dorsal view, showing T1–T2; f: Lateral surface of propodeum in lateral view, showing the short appressed hairs . Scale bar: 1mm.


not narrowed medially, wider than width of the exposed T1 (Fig 1c); sloping anterior and lateral anterior parts of

T1 covered with white erect long and numerous plumose hairs (Fig 1c); apical lobe of S7 rounded and enlarged

apically (Fig 1d); genitalia as showing in Fig 1e (in lateral view) and Fig 1f (in dorsal view). Antennal flagella

ventrally yellowish brown; distitarsi of all legs yellowish brown, other parts black. Face covered with dense long

white plumose hairs; gena, vertex, scutum, scutellum and mesepisternum covered with long white plumose hairs.

Female, BL=6.5mm (Fig 2a); head broader than long, HW:HL=50: 37 (Fig 2b); gena narrower than eye in lateral

view, GW:EW=7:11 (Fig 2c); width of metasoma slightly narrower that between tegulae, MtW:TW=45:45.

Clypeus nearly as long as broad, finely and densely punctate (Fig 2b); disc of scutum and scutellum smooth and

shiny, without punctation (Fig 2d); malar area medially only 1/3 long as width of mandible base; facial fovea

narrower than width of antennal flagellum, only 0.5 times as wide as antennal flagellum; propodeum laterally

densely covered with short appressed hairs that hide sculpture of integument (Fig 2f); punctation on disc of T1 fine,

round and dense, i=0.5–1.0d; T1–T4 with complete yellowish white apical hair bands, the apical band on T1

uninterrupted and not narrowed medially, T2 with broad yellowish white basal hair band, the band wider than the

exposed T2 (Fig 2e); sloping anterior and basal parts of T1 covered with yellowish white appressed long plumose

hairs, lateral anterior part of T1 covered with white erect long plumose hairs (Fig 2e). Antennal flagella ventrally

yellowish brown (Fig 2c); distitarsi of all legs dark brown, other parts black. Face covered with white long plumose

hairs, vertex, scutum, scutellum and mesepisternum covered with paler white long plumose hairs (Fig 2a).

Material examined. 4♂, 1♀, China, Qinghai, Dulan Xian, 2570km of G109 Road (96º39′E, 36º21′N), 2788m,

18.VII.2013, (Tamarix chinensis), coll. Qing-Tao Wu; 1♂, Qinghai, Dulan Xian, Nuomuhong (96º27′E, 36º23′N),

2844m, 29.VII.2013, coll. Qing-Tao Wu.

Published records. There are two old records of C. popovi from China mentioned by Noskiewicz (1936) who

described the species based on this material: 1♀ (Lectotype), “Szybendu Szuguza n. Satschóu, Gaschun - Gobi

[China: Gansu; 94°17É, 39°56Ń], 9–12/VIII.1895, Kozlow leg.”; 1♂, “Orogün (Zajdam in Gobi) [China:

Qinghai; 95°38É, 38°19Ń], 1–3/VII.1895, Kozlow leg.”. Shi et al. (2010) reported C. popovi as flower visitor of

Eremosparton songoricum (Fabaceae) at two sites near the village of Dure (Xinjiang) at 46°31′05″N, 88°33′04″E

and at 46°28′04″N, 88°33′04″E respectively. These specimens should be re-examined to check the correctness of

identification because of the taxonomic problems and the large number of similar species of other species-groups

in that region.

Distribution in China. Gansu, Qinghai (Fig 6).

General distribution. China, Kazakhstan, Mongolia.

Floral association. Tamarix chinensis (Tamaricaceae).

DNA Barcoding. We sequenced 3 specimens, with 2 females and 1 male. All three sequences from both sexes

were grouped together in a single highly supported branch (Fig 5).

Colletes vestitus sp. n.

(Figs 3a–f, male; 4a–f, female; 6)

Diagnosis. In the female of this species the abdominal terga are completely and densely covered with appressed

white hairs (Figs 4e, 4f), a character that within the C. flavicornis-group is only shared by C. alicularis Noskiewicz

and C. emaceatus Noskiewicz. From both species C. vestitus differs by its conspicuously raised clypeus (Fig 4d)

and the combination of black legs (at least partly yellowish-brown in C. emaceatus) and a sparsely punctate

clypeus (Fig 4c) (densely punctate in C. alicularis). In the male terga are also completely covered with appressed

white pilosity (Fig 3f) like in C. alicularis (male of C. pallipes Noskiewicz unknown). Both species are very

similar but in C. vestitus S7 more distinctly emarginate (Fig 3b) (almost linear in C. alicularis) and the gonostylus

is shorter but broader at its base (Fig 3d).

Description. Male, BL=6.0–6.5mm (Fig 3a); head broader than long, HW:HL=42:36; gena clearly narrower

than eye in lateral view, GW:EW=5:10; width of metasoma slightly narrower than that between tegulae,

MtW:TW=34:40. Antenna short, extending to scutellum, first flagellomere nearly as long as broad, 0.7 time as long

as second flagellomere, second flagellomere longer than broad, nearly 1.3 times as long as broad, flagellomeres 3–

11 roughly 1.4 times as long as broad and nearly equal to each other in length (Fig 3e); malar area medially about

2.0 times long as width of mandible base; facial fovea shallow and narrow, only 0.5 times as wide as antennal


FIGURE 3. Colletes vestitus sp. n., male. a: Body in lateral view; b: S7 in dorsal view; c: Genitalia in dorsal view; d: Genitalia in lateral view; e: Head in lateral view; f: T1–T2 in dorsal view. Scale bar: a, e, f, 1mm; b, c, d, 0.5mm.


FIGURE 4. Colletes vestitus sp. n., female. a: Body in lateral view; b: Mesonotum in dorsal view; c: Head in frontal view; d: Head in lateral view; e: Metasoma in dorsal view; f: T1–T2 in dorsal view. Scale bar: 1mm.


FIGURE 5. NJ tree based on the DNA barcode sequence of mitochondrial COI from different specimens of genus Colletes

from China. For details of the sequenced specimens see Table 2. The symbols of F and M represent the sex of specimens is female and male respectively.


FIGURE 6. Distribution map of Chinese species of the Colletes flavicornis-group. ●: Colletes popovi Noskiewicz, 1936; �: Colletes vestitus sp. n.

flagellum; propodeum laterally covered with sparse long erect hairs, integumental sculpture completely visible;

disc of scutum shallowly and sparsely punctate, i=2.0–3.5d, and disc of scutellum smooth and shiny, without

punctation; posterior margin of T1 yellowish brown (Fig 3f); disc of T1 dispersed and finely punctate, i=1.0–2.0d;

metasomal terga densely covered with long appressed white plumose pilosity (Figs 3a, 3f); sloping anterior and

lateral anterior parts of T1 covered with long white erect plumose hairs (Fig 3f); apical lobe of S7 medially

emarginate and enlarged apically (Fig 3b); genitalia as showing in Fig 3c (in dorsal view) and Fig 3d (in lateral

view). Antennal flagella ventrally yellowish brown (Fig 3e); tarsi of all legs yellowish brown, other parts black.

Face covered with dense long white plumose hairs; gena, vertex, scutum, scutellum and mesepisternum covered

with long white plumose hairs.

Female, BL=6.0mm (Fig 4a); head broader than long, HW:HL=47:38 (Fig 4c); gena clearly narrower than eye

in lateral view, GW:EW=5:12 (Fig 4d); width of metasoma narrower that between tegulae, MtW:TW=38:48.

Clypeus nearly as long as broad, obviously raised (Fig 4d), finely and sparsely punctate (Fig 4c); disc of scutum

smooth and shiny, marginal area of scutum finely and sparsely punctate, and scutellum smooth and shiny, without

punctation (Fig 4b); malar area medially nearly as long as width of mandible base (Fig 4d); facial fovea narrower

than width of antennal flagellum, only 0.5 times as wide as antennal flagellum; propodeum laterally covered with

sparse long erect hairs, integumental sculpture completely visible; posterior margin of T1 yellowish brown (Fig

4f); disc of T1 densely and finely punctate, i=0.5–1.0d (Fig 4f); sloping anterior and basal parts of T1 covered with

long white appressed plumose hairs, lateral anterior part of T1 covered with erect long white plumose hairs (Fig 4e,

4f); metasomal terga completely and densely covered with appressed white plumose hairs (Fig 4e). Antennal

flagella ventrally yellowish brown (Fig 4b, 4c); mediotarsi and distitarsi of forelegs, mediotarsi and distitarsi of

middle legs, and hind tarsi dark brown, other parts black. Face, vertex, scutum and mesepisternum covered with

long white plumose hairs (Fig 4c, 4d); scutum and scutellum covered with long paler white plumose hairs (Fig 4b).

Type material. Holotype: 1♀, China, Xinjiang, Fukang, Cainan (87º54′E, 44º06′N), 27.V.2013, coll. Liu-

Sheng Cheng; Paratypes: 1♀, 9♂, same label information as holotype.

Distribution. China: Xinjiang (Fukang, Cainan) (Fig 6).

Floral association. No record.


Etymology. The specific epithet is Latin vestitus, meaning the metasomal terga densely covered with plumose

hairs.

DNA Barcoding. We sequenced 10 specimens of this species, with 8 males and two females. All sequences

were grouped in the same highly supported branch to confirm the species identity of both sexes (Fig 5).

Acknowledgements

The authors wish to thank Prof. Yan-Ru Wu, Dr. Yan-Zhou Zhang for their help and encouragement throughout the

preparation of this paper, and for Dr. Douglas Chesters for revising the English language of parts of the manuscript.

The authors also wish to thank Dr. Claus Rasmussen and Maxim Proshchalykin for their comments on the earlier

drafts of the manuscript. We also appreciate the help of Qing-Tao Wu and Liu-Sheng Cheng, who made the rich

collection for our study, and Qing-Yan Dai who sequenced DNA barcodes.

This work was supported mainly by grants from the National Science Foundation, China (Grants Nos.

31272264, J0930004) and the National Specific Research Funds for Public Benefit Department (Agriculture)

(Grant No. 201303108) to Ze-Qing Niu, the National Science Foundation, China (Grants Nos. 30870268,

31172048, J1211002) and the grant from Key Laboratory of Zoological Systematics and Evolution, Chinese

Academy of Sciences (No. Y229YX5105) to Chao-Dong Zhu.

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http://dx.doi.org/10.1093/molbev/msr121

bees of the colletes flavicornis-group from china with description of one new species (hymenoptera:...

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