A species checklist of the subgenus Culicoides (Avaritia) in China, with a description of a new species (Diptera, Ceratopogonidae).

A checklist of the subgenus Culicoides (Avaritia Fox) (Diptera: Ceratopogonidae: Culicoides) in China, currently including 57 species, is provided. Their full citations, more detailed locations of the type locality, and distribution of each species by province, and/or state of each species are also provided. Culicoides (Avaritia) fenggangensis Liu & Hou, sp. n. is described and illustrated, based on both male and female specimens from China. The new species is compared with its similar congeners, C. (A.) comparis Liu & Yu, 2005 and C. (A.) dentiformis McDonald & Lu, 1972.

Introduction

Biting midges of the genus Latreille (, ) are found everywhere in the world and females are the smallest of insect vectors (Mellor et al. 2000). Some species of spread disease in humans and livestock as vectors of arboviruses, such as bluetongue virus (BTV), Schmallenberg virus (SBV), and others (Borkent PageBreak2005), which leads to direct economic costs for agriculture (Gibbens 2012; Velthuis et al. 2010). In China, Bluetongue has been recorded from several provinces in south, such as Yunnan, Hubei, Anhui, Sichuan, Shanxi and so on (Zhang et al. 2015), and the vector of BTV mainly distributed in the south region of north latitude 40° (Zhang et al. 2014). Therefore, members of this genus have great international significance and have attracted more scientific attention in recent years. The genus , currently with a total number of species of 1415 in the world, 1368 extant species and 47 fossil species (Borkent, 2016), has 348 species in China. Many of the important vectors are in the subgenus Fox). The purpose of this paper is to provide a checklist of this subgenus in China, and describe and illustrate sp. n.

Materials and methods

The specimens were collected with light traps near households in the mountains of Fenggang County of Guizhou Province. For microscopic observation, specimens were preserved in 100% ethanol and then slide-mounted in Canada balsam following the technique described by Yu et al. (2005). Diagnostic features were microphotographed using an Imaging System of Upright Research Microscope adapted to a microscope (Nikon Eclipse Ni-E) and a Digital System of Large depth-of-field 3D Digital Microscope (Keyence VHX-1000C), and Photoshop CS4 was used to obtain the final images. Morphological terms are from the chapter on by Yu et al. (2005). Terms of structures specific to follow those described by Santarém et al. (2014) and Han et al. (2017). Measurements of wings, flagellar segments, palpus, and legs are given in millimeters, and measurements of spermathecae are given in microns. Meristic information is presented as ranges of values, followed by mean and sample size. The type specimens are deposited in Insect Collection of Zunyi Medical University, Guizhou Province, China.

Taxonomy

Checklist of the subgenus in China in alphabetical order

Subgenus

Fox, 1955: 218.

Type species. Meigen, 1818.

Dzhafarov, 1964: 263; Liu et al. 2011: 385. Type Locality: Georgia.

Distribution. China (Liaoning); Georgia.

Smith, 1929: 255; McDonald and Lu 1972: 411; Lee 1988: 29; Yu et al. 2005: 907. Type locality: India.

Arnaud, 1956: 119. Type locality: Japan.

Das Gupta, 1962a: 538. Type locality: India.

Distribution. China (Heilongjiang, Jiangsu, Anhui, Fujian, Taiwan, Shandong, Hubei, Guangdong, Guangxi, Hainan, Sichuan, Yunnan, Tibet, Shaanxi, Hunan); India, Indonesia, Malaysia, Philippines, Vietnam, Japan, Thailand.

Tokunaga, 1937: 319; Lee 1978: 28; Yu et al. 2005: 908. Type locality: China: Taiwan.

Distribution. China (Heilongjiang, Tibet, Sichuan, Yunnan, Taiwan).

Yu, Wang & Chen, in Wang et al., 2012: 283. Type Locality: China: Hainan, Bawangling.

Distribution. China (Hainan).

Delfinado, 1961: 654; Yu et al. 2005: 910. Type locality: Philippines.

Distribution. China (Taiwan, Guangdong, Hainan, Yunnan); Australia, Indonesia, Malaysia, Japan, Sri Lanka, Thailand, Philippines.

Kieffer, 1917: 187; Yu et al. 2005: 911. Type locality: Australia.

Lee & Reye, 1953: 386. Type locality: Australia.

Delfinado, 1961: 657. Type locality: Philippines.

Das Gupta, 1962b: 253. Type locality: India.

Distribution. China (Anhui, Taiwan, Hainan); Australia, Philippines, India, Laos, Malaysia.

Delfinado, 1961: 658; Yu et al. 2005: 913. Type locality: The Philippines.

Distribution. China (Taiwan), Philippines.

Meigen, 1830: 263. Type locality: Europe.

Winnertz, 1852: 35. Type locality: Germany.

Goetghebuer, 1927: 203. Type locality: Belgium.

Callot & Kremer, 1969: 610. Type locality: France.

Distribution. China (Hebei, Inner Mongolia, Liaoning, Jilin, Heilongjiang, Tibet); Germany, France, Belgium, Britain, Russia.

Mukerji, 1931: 1052; McDonald and Lu 1972: 403; Yu et al. 2005: 916. Type locality: India.

Sen & Das Gupta, 1959: 620. Type locality: India.

Distribution. China (Jiangsu, Fujian, Shandong, Hainan, Sichuan); India, Indonesia, Laos, Malaysia, Philippines, Thailand.

Liu & Yu, in Yu et al., 2005: 917. Type locality: China: Tibet, Nielamu.

Distribution. China (Tibet).

Liu & Yu, 1990: 19; Yu et al. 2005: 919. Type locality: China: Tibet, Cuona.

Distribution. China (Tibet).

McDonald & Lu, 1972: 403; Yu et al. 2005: 921. Type locality: China: Taiwan.

Distribution. China (Taiwan).

Chu & Liu, 1978: 83; Yu et al. 2005: 922. Type locality: China: Yunnan, Mengla.

Distribution. China (Fujian, Yunnan).

Liu & Hou, sp. n., this paper. Type locality: China: Guizhou, Fenggang.

Distribution. China (Guizhou).

Gornostaeva & Gachegova, 1972: 522; Yu et al. 2005: 924. Type locality: Russia.

Distribution. China (Tibet, Heilongjiang); Russia.

Yu, 1982: 202; Yu et al. 2005: 925. Type locality: China: Hainan, Diaoluoshan.

Distribution. China (Hainan).

Lee, 1980: 85; Yu et al. 2005: 927. Type locality: China: Yunnan.

Distribution. China (Yunnan).

Wirth & Hubert, 1961: 16; Yu et al. 2005: 928. Type locality: China: Taiwan.

Distribution. China (Taiwan, Guangdong, Hainan, Yunnan, Hunan); Indonesia, Laos, Malaysia.

Kieffer, 1913: 11; Yu et al. 2005: 930. Type locality: Kenya.

Carter, Ingram & Macfie, 1920: 265. Type locality: Ghana.

Khalaf, 1957: 343. Type locality: Iraq.

Sen & Das Gupta, 1959: 622. Type locality: India.

Das Gupta, 1962a: 537. Type locality: India.

Distribution. China (Hainan); Wide spread in Africa, the Middle and Far East, India, Laos, Sri Lanka, Vietnam.

Yu & Zhang, in Yu, 1988: 136; Yu et al. 2005: 931. Type locality: China: Tibet.

Distribution. China (Tibet).

Sen & Das Gupta, 1959: 626; Yu et al. 2005: 933. Type locality: India.

Distribution. China (Hainan); India, Cambodia, Indonesia, Laos, Malaysia, Sri Lanka, Thailand.

Macfie, 1937b: 469; Lee 1988: 65; Yu et al. 2005: 935. Type locality: Malaysia.

Distribution. China (Fujian, Taiwan, Yunnan, Hunan); Malaysia, Brunei, Indonesia, Laos, Philippines, Singapore, Thailand.

Zhou & Lee, 1984: 295; Yu et al. 2005: 936. Type locality: China: Chongqing.

Distribution. China (Chongqing).

Macfie, 1934: 215; Yu 1982: 48. Yu et al. 2005: 938. Type locality: Indonesia.

Macfie, 1937a: 117. Type locality: Malaysia.

Tokunaga, 1955: 6. Type locality: Japan.

Tokunaga, 1959: 236. Type locality: Papua New Guinea.

Distribution. China (Fujian, Taiwan, Guangdong, Guangxi, Hainan, Yunnan, Tibet, Hunan); Indonesia, Malaysia, Japan, New Guinea, Philippines, Thailand.

Lee, 1988: 69; Wirth and Hubert 1989: 346; Yu et al. 2005: 940. Type locality: China; Malaysia.

Distribution. China (Fujian, Taiwan); Malaysia, Laos, Thailand.

Wirth & Hubert, 1989: 211; Yu et al. 2005: 941. Type locality: Indonesia.

Distribution. China (Hainan).

Howarth, 1985: 58; Liu et al. 1996: 38; Yu et al. 2005: 942. Type locality: Laos.

Distribution. China (Guangdong, Hainan, Hunan).

Yu & Liu, 1990: 10; Yu et al. 2005: 944. Type locality: China: Guangdong, Shixing.

Distribution. China (Guangdong).

Wirth & Hubert, 1961: 20; Yu et al. 2005: 946. Type locality: China: Taiwan.

Distribution. China (Taiwan, Yunnan); Indonesia, Laos, Malaysia, Philippines, Thailand.

Qu & Wang, 1994: 486; Yu et al. 2005: 947. Type locality: China: Tibet.

Distribution. China (Tibet).

Macfie, 1937b: 471; Yu 1982: 190; Yu et al. 2005: 949. Type locality: Malaysia.

Distribution. China (Fujian, Taiwan, Guangdong, Guangxi, Hainan, Yunnan); Indonesia, Malaysia, Philippines, Thailand.

Lee, 1979: 101; Yu et al. 2005: 951. Type locality: China: Tibet, Cuona.

Distribution. China (Sichuan, Tibet).

Lee, 1978: 75; Yu et al. 2005: 952. Type locality: China: Tibet, Motuo.

Distribution. China (Tibet).

Liu & Deng, 2000: 246; Yu et al. 2005: 954. Type locality: China: Tibet, Nielamu.

Distribution. China (Tibet).

Fei & Lee, 1984: 345; Yu et al. 2005: 955. Type locality: China: Inner Mongolia, Linxi.

Distribution. China (Inner Mongolia).

Liu, 1990: 59; Yu et al. 2005: 956. Type locality: China: Yunnan, Nujiang.

Distribution. China (Yunnan).

Meigen, 1818: 76. Type locality: Europe.

Winnertz, 1852: 35. Type locality: Germany.

Matsumura, 1911: 60. Type locality: Russia.

Santos Abreu, 1918: 297. Type locality: Spain.

Kieffer, 1919a: 47. Type locality: Slovak Republic, Ukraine.

Kieffer, 1921: 56. Type locality: Germany.

Kieffer, 1921: 56. Type locality: Germany.

Kieffer, 1921: 57. Type locality: Germany.

Kieffer, 1922: 235. Type locality: Germany.

Kieffer, 1922: 505. Type locality: Algeria.

Kieffer, 1922: 71. Type locality: Germany.

Okada, 1941: 22. Type locality: Japan.

Cambournac, 1956: 591. Type locality: Portugal.

Shevchenko, 1967: 173. Type locality: Ukraine.

Distribution. China (Shanxi, Inner Mongolia, Liaoning, Jilin, Heilongjiang, Fujian, Shandong, Sichuan, Chongqing, Yunnan, Xinjiang, Gansu, Tibet); wide distribution in Palaearctic Region, Britain, Germany, Russia, Canary Islands, Algeria, Japan, Portugal, Slovakia, Ukraine.

Wirth & Hubert, 1989: 222; Yu et al. 2005: 959. Type locality: Malaysia.

Distribution. China (Hainan); Malaysia.

Macfie, 1932: 490; Lee 1978: 83; Yu et al. 2005: 961. Type locality: Malaysia.

Das Gupta, 1963: 35. Type locality: India.

Distribution. China (Fujian, Taiwan, Hainan, Sichuan, Yunnan, Tibet, Hunan); Malaysia, India, Indonesia, Philippines, Thailand, Vietnam, the Solomon Islands.

Tokunaga, in Tokunaga & Murachi, 1959: 348; Yu 1982: 57; Yu et al. 2005: 963. Type locality: USA.

Distribution. China (Guangdong, Hainan, Yunnan); Oceania.

Kitaoka, 1980: 11; Lee 1988: 91; Yu et al. 2005: 964. Type locality: Japan.

Distribution. China (Sichuan, Yunnan); Japan.

Liu & Yu, 1990: 23; Liu and Deng 2000: 245; Yu et al. 2005: 966. Type locality: China: Tibet, Cuona.

Distribution. China (Tibet).

Kieffer, 1910: 191; Yu et al. 2005: 967. Type locality: India.

Bezzi, 1916: 8. Type locality: Philippines.

Salm, 1917b: 136. Type locality: Indonesia.

Kieffer, 1921: 564. Type locality: Philippines.

Smith & Swaminath, 1932: 183. Type locality: India.

Tokunaga, 1951: 108. Type locality: Indonesia.

Distribution. China (Hebei, Inner Mongolia, Liaoning, Jiangsu, Fujian, Taiwan, Jiangxi, Henan, Guangdong, Guangxi, Hainan); India, Philippines, Indonesia.

Yu & Liu, 1990: 4; Yu et al. 2005: 969. Type locality: China: Sichuan, Xichang.

Distribution. China (Sichuan).

Lee, 1980: 86; Yu et al. 2005: 971. Type locality: China: Yunnan.

Distribution. China (Yunnan).

Downes & Kettle, 1952: 65; Yu et al. 2005: 972. Type locality: Great Britain.

Distribution. China (Tibet); Great Britain, France.

Tokunaga, 1937: 331; Yu et al. 2005: 973. Type locality: Japan.

Amosova, 1957: 233. Type locality: Russia.

Distribution. China (Liaoning, Jilin, Heilongjiang, Yunnan, Shaanxi); Japan, Russia.

Hou, Han, Lv & Jiang, 2014: 98. Type Locality: China: Guizhou, Suiyang.

Distribution. China (Guizhou).

Macfie, 1934: 190; Yu et al. 2005: 975. Type locality: Malaysia.

Tokunaga, 1937: 325. Type locality: Japan.

Tokunaga, 1937: 327. Type locality: Taiwan.

Takahashi, 1958: 113. Type locality: Japan.

Delfinado, 1961: 660. Type locality: Philippines.

Distribution. China (Fujian, Taiwan, Guangdong, Guangxi, Hainan, Yunnan, Tibet); Malaysia, Japan, Philippines.

Kitaoka, 1973: 212; Lee 1988: 107; Yu et al. 2005: 977. Type locality: Japan.

Distribution. China (Taiwan, Yunnan); Japan.

Kieffer, 1916: 114; Yu et al. 2005: 979. Type locality: China: Taiwan.

Shiraki, 1913: 294. Type locality: China: Taiwan.

Tokunaga, 1937: 284. Type locality: Japan.

Tokunaga, 1937: 322. Type locality: Japan.

Tokunaga, 1937: 329. Type locality: Japan.

Tokunaga, 1951: 106. Type locality: Indonesia.

Distribution. China (Fujian, Hainan, Yunnan, Shaanxi, Shandong); Indonesia, Japan, Laos, Malaysia, Philippines, Thailand, Vietnam.

Chu, 1977: 102; Yu et al. 2005: 980. Type locality: China: Tibet.

Distribution. China (Sichuan, Tibet).

McDonald & Lu, 1972: 415; Yu et al. 2005: 982. Type locality: China: Taiwan.

Distribution. China (Taiwan).

Kitaoka, 1980: 14; Yu et al. 2005: 984. Type locality: China: Taiwan.

Distribution. China (Fujian, Guangxi, Taiwan).

Wang & Liu, 1999: 328; Yu et al. 2005: 985. Type locality: China: Heilongjiang, Raohe.

Distribution. China (Heilongjiang).

Lien, Lin & Weng, 1998: 57; Yu et al. 2005: 987. Type locality: China: Taiwan, Lanyu.

Distribution. China (Taiwan).

Lien, Lin & Weng, 1998: 58; Yu et al. 2005: 988. Type locality: China: Taiwan.

Distribution. China (Taiwan).

Liu & Hou sp. n.

http://zoobank.org/52A53C15-0F18-4040-B83C-B678BD2E9A66

Figs 1 , 2 , 3

Figure 1.

sp. n. Left Wing. a Female b Male.

Figure 2.

a–j sp. n. a Head, anterior view b Eye contiguous, anterior view c Left palpus, anterior view d Right palpus, anterior view e Mandibular teeth f Thorax and legs, lateral view g Apex of hind tibia and base of first tarsomere, posterior view. h Apex of hind tibia and base of first tarsomere, posterior view. i Spermathecae j Genitalia, ventral view (Female: a–c, e–i; Male: d, j).

Figure 3.

sp. n. a Genitalia and aedeagus (parameres absent), ventral view b parameres, ventral view.

Diagnosis.

Male: only species of in China with the following combination of features: the 3rd segment of the palpus is slender, PR 3.11; the apex of 9th tergite has lateral processes; parameres with apical portion elongate, bent abruptly; aedeagus nearly triangular, with a long ovoid process at its apex. Female: only species of in China with the following combination of features: cell m2 with four sparsely distributed pale spots; the 3rd segment of the palpus is slender, PR 3.20–3.75.

Description.

Female. Head (Fig. 2a). Brown. Eyes (Fig. 2b) contiguous, abutting medially for length of 1.5 ommatidia, with interfacetal hairs. Antennal pedicel brown; Lengths of antennal flagellomeres in proportion of 19: 14: 14: 15: 15: 15: 16: 17: 25: 25: 25: 31: 47; AR 1.22–1.28 (1.24, n = 3); sensilla coeloconica on flagellomeres 1, 9–13. 3rd segment of palpus slender, slightly swollen at apical 1/3, with small, rounded sensory pit (Fig. 2c–d); PR 3.20–3.75 (3.45, n = 3). Mandible with 14–18 (16, n = 4) teeth (Fig. 2e); Maxilla with 17 teeth (n = 3); P/H ratio 1.04–1.17 (1.11, n = 3).

Thorax (Fig. 2f). Dark brown. Scutellum without distinct pattern in slide-mounted specimens. Wing (Fig. 1a) with contrasting pattern of pale, dark spots; distal 1/2 of 1st, proximal 1/2 of 2nd radial cell in dark spot; three pale spots near anterior margin: 1st over base of cell r1 and r-m crossvein extending from below M1 to margin of costa, 2nd over distal of cell r2 from dorsal portion of M1 to costa, 3rd morphological variation, from dorsal portion of M1 to just below costa; cell m1 with two separated pale spots: one spot small, ovoid, another large, triangle, far from distal portion of wing; cell m2 with four different shapes, sizes pale spots: 1st proximal to CuA, 2nd between medial and mediocubital forks, 3rd and 4th below M2, latter reaching wing margin; cua1 with a large, ovoid pale spot abutting wing posterior margin; anal cell with two pale spots: proximal pale spot on Cu2 and CuA, distal pale spot near mediocubital fork; wing base with faint pale spot on M; macrotrichia sparsely distributed on distal 1/3 of wing, but not in basal cell; wing length 1.45–1.60 (1.52, n = 3) mm, width 0.68–0.73 (0.70, n = 3) mm; CR 0.55–0.59 (0.57, n = 3). TR and F-T of legs (Fig. 2f) are given as Table 1, metatibial distal bristles (Fig. 2g–h) with 5 or 6 spines, 1st spine is longest.

Table 1.

Tarsal ratios (TR) and measurements of leg segments and tarsomeres from femur to tarsomere 5 (F-T) of all legs of sp. n. (♀).

Leg	TR	F-T
Foreleg	2.12	85 : 88 : 53 : 25 : 16 : 10 : 11
Midleg	2.31	109 : 114 : 60 : 26 : 16 : 10 : 11
Hindleg	1.73	109 : 115 : 57 : 33 : 17 : 11 : 12

Abdomen. Brown. Two subequal-size ovoid spermathecae (Fig. 2i), measuring 65.0–72.5 × 50.0–57.5 (n = 3) μm, 65.0–72.5 × 50.0 (n = 2) μm, slender sclerotized necks with 2.5–7.5 (n = 3) μm; third slender, elongate rudimentary spermatheca, length 20.0–25.0 (n = 3) μm.

Male. Similar to female with usual sexual differences. Sensilla coeloconica on flagellomeres 1, 11–13; AR 0.87 (n = 1); PR 3.11 (n = 1). Wing with pattern of pale spots as in PageBreakFig. 1b, wing length 1.58 (n = 1), width 0.55 (n = 1); CR 0.57 (n = 1). TR and F-T of legs are given as Table 2. Genitalia (Fig. 2j): 9th tergite squarish, distal portion flat with short, conical processes at apicolateral. Ninth sternite with broad, deep, semicircle caudomedian excavation. Gonocoxite twice as long as broad, sclerotized; gonostylus tapering distally, distal portion curved. Parameres (Fig. 3b) separate, contiguous in midportions; each with moderately long, slender basal arm, swollen at base, stem long, slightly curved near base; apical portion tapered, elongate, abruptly bent without lateral fringe of spicules. Aedeagus (Fig. 3a) nearly triangle, basal arms short, unciform, tapering toward end, basal arch low, extending to 1/5 of total length, distal process 1/6 total length, long ovoid process at apex.

Table 2.

TR and F-T of all legs of sp. n. (♂).

Leg	TR	F-T
Foreleg	2.67	95 : 92 : 56: 21 : 15 : 8 : 9
Midleg	1.94	115 : 112 : 64 : 33 : 16 : 8 : 9
Hindleg	1.49	117 : 117 : 55 : 37 : 19 : 9 : 10

Type material. Holotype female, Chongxin village, Yong’an town, Fenggang county, Zunyi city, Guizhou province, China (), 12. IV. 2016, alt. 908m, Qiongqiong Chang col. Paratypes: 2 males and 3 females, same data as holotype.

Distribution.

China (Guizhou Province).

Etymology.

This species is named in tribute to Fenggang county, where the specimens were collected.

Taxonomic discussion

sp. n. is very similar to Liu & Yu, 2005 and McDonald & Lu, 1972 based on the interfacetal hairs PageBreakon the eyes and sensilla coeloconica on the flagellomeres. sp. n. can be distinguished from these two congeners by the number and distribution of pale spots on the wing (cell m2 with two and three pale spots respectively in and ) (Yu et al. 2005), elongate and cylindrical third palpus segment (third palpus segment is swollen in and ). Females of sp. n. have a different wing size (wing length 1.33 mm and width 0.63 mm in and wing length 1.78 mm and width 0.76 mm in ), distribution of the heavy macrotrichia on the wing (respectively distal 4/5 and 1/4 of the wing in and ), they have a more slender 3rd palpus segment compared to the most species of subgenus (only 12 species PR > 3.2), PR 3.2–3.75 (respectively PR 2.27 and 2.5 in and ), different size of spermathecae (measuring 45.0 × 40.0 μm in and 60.0 × 45.0 μm in ). Because male of is unknown, the new species will only compare with . Males of sp. n. have a different shape and structure of genitalia, with two lateral processes on the distal portion of ninth tergite (without lateral process in ), parameres apical portion tapered and abruptly bent (linear in ), long ovoid process at apex of aedeagus (diamond-shape process in ). Therefore, the distinctive features to separate sp. n. from others are cell m1 and m2 with 2 and 4 pale spots respectively.

The male of keys to in Yu et al. (2005) where it may be distinguished by the presence of conical apicolateral processes on tergite 9 which are absent in . The female of keys to the couplet with and in Yu et al. (2005) where it may be distinguished by the presence of 4 pale spots in cell m2 which are absent in and .

The biogeographical territory of China spans the Palaearctic and Oriental Regions, which results in a rich diversity of biting midge species. The species of the subgenus are distributed in most provinces of China, except Qinghai and Ningxia. There are 15 species distributed in the Palaearctic Region, accounting for 26.3% of the total (, , , , , , , , , , , , , , ). There are 49 species present in the Oriental Region, accounting for 86.0% of the total (, , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , ). Finally, there are seven species present in both Regions, accounting for 12.3% of the total. This geographical distribution of biting midges in China is consistent with the distribution of other animals (Yan and Yu 1998).