Culicoides brevitarsis Kieffer

Bellis, Glenn, Dyce, Alan, Gopurenko, David, Yanase, Tohru, Garros, Claire, Labuschagne, Karien & Mitchell, Andrew, 2014, Revision of the Culicoides (Avaritia) Imicola complex Khamala & Kettle (Diptera: Ceratopogonidae) from the Australasian region, Zootaxa 3768 (4), pp. 401-427 : 405-407

Culicoides brevitarsis Kieffer

( Figs 2, 6, 7, 10, 11 , 13, 16, 19 , 22, 24, 26, 29, 32 , 37, 38, 39, 44)

Culicoides brevitarsis Kieffer 1917: 187 ; Lee & Reye 1962:362 ( C. robertsi synonymy); Kettle & Elson 1976: 313 (description of larva and pupa); Dyce 1979: 52 ( C. radicitus synonymy); Dyce & Wirth 1983: 224 ( C. superfulvus synonymy); Wirth & Hubert 1989: 258 (description of male and female, SE Asian records; designation of neotype); Lien et al., 1998:27 (misident. Taiwan record, description of male and female). Yu et al. 2005:911 (redescription of male and female, China record); Dyce et al., 2007:19 (female wing illustrated).

Culicoides robertsi Lee & Reye 1953:386 ; Tokunaga, 1960:74 ( C. orientalis male of Tokunaga 1959 misdet.); Tokunaga, 1962:485 (male and female redescribed; New Guinea and Solomon Islands);

Culicoides radicitus Delfinado 1961:657 (in part).

Culicoides superfulvus Das Gupta 1962:253

Culicoides orientalis Macfie (misident.); Tokunaga, 1959:254 (Indonesian Papua record).

Type material examined. C. radicitus : Philippines Tala, Rizal, 21.v.1958, M Delfinado, (neotype male for C. brevitarsis , designation by Wirth & Hubert 1989, USNM).

C. superfulvus : India Baguiati (near Calcutta) by sticky trap, August, ’60, Das Gupta (cotype female, designation by Dyce & Wirth 1983, USNM). C. brevitarsis : Australia, NSW. (neoallotype female, Lismore, 13.Nov.2007, H. McKenzie, ANIC).

Non-type material examined. Australia. NSW: Paterson, 6.Feb.2008, Lt Tp. (1 female, NTQIC); NSW, Grafton, 14.Dec.2007, H. McKenzie (1 female, NTQIC); Qld: Oxley Ck, Corinda, 18.March.2009, M. Shivas, (1 female, NTQIC); Bamaga, 27.Jan.2009, J Sailor, (1 female, NTQIC). Timor Leste, Surucraic, 9.05583°S; 125.5444°E, 15.Nov.2001, Lt Tp, E. Watkins, (1 female, NTQIC); 4 km. N. Same, Lt. Tp. 24th Aug 1969, D. Nicholls (3 females, ANIC); Cape Tefara, lt. tp. 5th Aug 1969, DG. Nicholls (1 female, ANIC); Cape Tefara, 11km. S.E. Suai, Lt. Tp. 6th August 1969, D. Nicholls (2 females, ANIC); Cape Tefara, lt. tp. 5th Aug 1969, DG. Nicholls (1 female, ANIC); Los Palos, lt. tp. 6–7.ix.69, DG. Nicholls (1 female, ANIC); Desa Pollo, 13 Sept 1984, Light trap, NT. Hunt (3 females, ANIC); Desa Pollo, 12–13 Sept 1984, NT. Hunt & Phillip, light trap by penned cattle (1 female, ANIC); Oecusse, Samora, 22.Feb.2005, G. Bellis (1 female, NTQIC); Cova Lima, Suai, 9.31°S, 125.26°E, 3.Dec.2003, E. Watkins (1 female, NTQIC);. Solomon Islands, Malaita, Kwailatutu, 8°56’24’’S, 160°46’43”E, 18.May.2010, L. Halling (1 female, NTQIC); Western Province, Tuiai via Nila,. 7.09491°S, 155.86068°E, light trap on edge of mangroves with 1 penned pig and 3 cattle, 0m, 19.Feb.2012, G. Bellis (3 females, NTQIC). Papua New Guinea, West New Britain, Numondo, 5°31.0'S, 150°5.0'E, 28.Feb.2007 LT, P. Boland, (1 female, NTQIC); Markham Farm, 6°32.684'S; 146°38.724'E, 11–17.June.2008, Lt Tp, J. Schmidt & N. Harris, (1 male, NTQIC). Indonesia, Bali, Denpasar, 9.Feb.1989, L.T. over cattle, HA. Standfast (2 females, 1 male, ANIC); Pedang bay, Denpasar, 35km NE, 17.Oct.1969, DG. Nicholls (1 female, ANIC). Kalimantan, 80-0818-29, VLi-95, V. Lee (1 female, ANIC). Flores, 80-0812-5, VLi-30, V.Lee (2 females, ANIC). Sumbawa, 22.Oct.1969, DG Nicholls (3 females, ANIC). West Timor, Kupang, Quarantine Station, L.T. over cattle, 7.Feb.1989, HA. Standfast (3 females, ANIC). Papua, Merauke, L.T. 15.Feb.89, HA Standfast, ov. cattle (7 females, ANIC). Thailand, Chiengmai, Apr- May 1958, V. Notananda, light trap (1 female, 1 male, ANIC). China, Hainan, Mengnya, 20.08°S, 110.37°E, Lt Tp, 28.Nov.2010, G. Bellis (2 males, NTQIC); Sanlian Can, 20.08°S, 110.37°E, Lt Tp, 28.Nov.2010, G. Bellis (1 male, NTQIC).

Diagnosis. We have been unable to reliably distinguish the morphology of C. brevitarsis from C. bolitinos Meiswinkel so the following diagnosis applies to both of these species and separates these two species from the remaining species in the Imicola complex. Female: The only species in the Imicola complex with the combination of wing with posterior margin of apical pale marking in cell m1 straight and never attaining vein M2 before margin of the wing, proximal dark marking on costa not longer than stigmatic dark spot and apical fifth of cell r2 included in post-stigmatic pale spot. Male: The only species in the Imicola complex with the combination of wing with posterior margin of apical pale marking in cell m1 straight and never attaining vein M2 before margin and proximal dark marking on costa no more than 1.5 times as long as the stigmatic dark spot.

Description. Adult. In addition to characters listed in the diagnosis, palpus ( Fig. 13 ) with 3rd segment bearing shallow pit of diameter about ½ width of segment and containing few, elongate, capitate sensilla; wing ( Fig. 6, 7 ) relatively strongly patterned with about 1/5 of cell r2 included in the post-stigmatic pale marking; legs ( Fig. 19 ) pale brown, hind femora unbanded, mid and fore femora with subapical pale band, all tibiae with pale subbasal band, mid & hind tibia additionally with weak pale apical bands; haltere pale. Male hypopygium (Fig. 37) with ninth sternite with ventral membrane bare. Aedeagus (Fig. 39) with peg strongly sclerotised and quite dark.

Immatures. Fourth instar larvae and pupae were adequately described by Kettle & Elson (1976).

Distribution. ( Fig. 44 ) Widespread in the Oriental and Australasian regions. Australia: NSW, Qld, NT, WA; PNG, Solomon Is, Fiji, New Caledonia, Vanuatu, Tonga, Timor Leste, Indonesia, Philippines, Thailand, China and India. Records from within the Oriental Region require confirmation as they may refer to C. asiatica .

Biology. Closely associated with bovids. Immatures live in discrete bovid dung pats ( Canon & Reye 1966, Campbell & Kettle 1976) while adults feed on sheep, cattle, marsupial, buffalo, human and horse (Lee et al. 1962; Kay 1973; Muller & Murray 1977; Muller et al. 1981; Kay & Lennon 1982). Adults are crepuscular ( Campbell & Kettle 1979b; Bellis et al. 2004), roost in ground herbage during daylight hours ( Bishop et al. 1995) and mate in swarms at sunset ( Campbell & Kettle 1979a). This species has been implicated in the transmission of 19 different viruses, including several of economic importance ( Doherty et al. 1972, St George et al. 1977, 1978, 1979, 1983; Muller et al. 1982; Zakrewski & Cybinski 1984; Parsonson & Snowdon 1985; Standfast et al. 1985; Cybinski & Muller 1990).

Remarks. Lee & Reye (1962) suggested the holotype specimen of C. brevitarsis may have been destroyed in the fire at the National Museum of Hungary in Budapest in 1956. Debenham (1979) was unable to locate the holotype specimen of this species confirming that it was lost in 1956 and prompting Wirth & Hubert (1989) to designate a neotype using the neotype male of C. radicitus . The designation of an allotype female from the type locality in Australia is however, desirable due both to the marked sexual dimorphism in wing pattern of this species and the confusion surrounding the identity of this species in Asia. Kieffer (1917) gave only “ Australie ” as the type locality but morphological and genetic analyses of C. brevitarsis from various localities in Australia (this study, Gopurenko et al. in preparation) has revealed there to be only a single species present indicating that any locality within Australia is suitable for an allotype specimen.

Within the Imicola group, C. brevitarsis is morphologically most similar to the African C. bolitinos and the Asian C. asiatica and this grouping is strongly supported by the molecular data. The relative lengths of the first and second dark marking along the costa enables reliable separation of C. brevitarsis and C. bolitinos from C. asiatica , but does not enable separation between C. brevitarsis and C. bolitinos . Meiswinkel (1995:31) offered the length:width ratio of flagellomeres 4–7 and the absolute length of all flagellomeres of the female antenna as a means of distinguishing C. brevitarsis from C. bolitinos . Data for these characters for C. asiatica , C. brevitarsis and C. bolitinos ( Table 6 ) illustrate that although differences are apparent between the mean values of these characters, the overlap evident between species makes identification of individual specimens unreliable. These three taxa are however, reliably separated using either the COI and CAD genes ( Fig. 46–48 ). Despite the closer morphological similarity of C. brevitarsis to C. bolitinos than to C. asiatica , both CAD and COI analyses indicate that C. asiatica is the sister species of C. brevitarsis ( Fig. 46–48 ).

Although COI analysis suggests that the Chinese specimens of C. brevitarsis may represent a further cryptic species ( Fig. 47 ), this was not supported by the CAD analysis, which nested these specimens among other genotypes of C. brevitarsis ( Fig. 48 ) suggesting that the COI division between Chinese and Australasian specimens reflects maternal phylogeographic structuring within the species rather than indicating presence of separate cryptic species.

Figures

FIGURE 46. Maximum likelihood tree inferred from concatenated CAD & COI sequences at Culicoides species in the Imicola complex and other representative Avaritia. Terminal labels indicate specimen ID and species (Table 7). Tree rooted at C. orientalis. Scale bar = 0.05 substitutions per site. Node support values generated from 1200 replicate ML searches (values <60 % not shown). Bayesian phylogenetic analysis pp supports estimated from 15000 sampled trees are indicated in the tree as circles at nodes, where closed circles represent> 98 % pp and open circles represent 70 – 98 % pp.

FIGURE 47. Maximum likelihood tree inferred from COI sequences at Culicoides species in the Imicola complex and other representative Avaritia. Terminal labels indicate specimen ID and species (Table 7). Tree rooted at C. orientalis. Scale bar = 0.05 substitutions per site. Node support values generated from 1200 replicate ML searches (values <60 % not shown). Bayesian phylogenetic analysis pp supports estimated from 15000 sampled trees are indicated in the tree as circles at nodes, where closed circles represent> 98 % pp and open circles represent 70 – 98 % pp. Specimen AY 286329 Culicoides pseudopallidipennis accessed from GenBank.

FIGURE 48. Maximum likelihood tree inferred from concatenated CAD sequences at Culicoides species in the Imicola complex and other representative Avaritia. Terminal labels indicate specimen ID and species (Table 7). Tree rooted at C. orientalis. Scale bar = 0.05 substitutions per site. Node support values generated from 1200 replicate ML searches (values <60 % not shown). Bayesian phylogenetic analysis pp supports estimated from 15000 sampled trees are indicated in the tree as circles at nodes, where closed circles represent> 98 % pp and open circles represent 70 – 98 % pp.

FIGURES 1 – 11. Culicoides (Avaritia) Imicola complex species. C. asiatica Bellis sp. n., 1, female eye separation; 4, female wing; 5, male wing. C. brevitarsis Kieffer, 2, female eye separation; 6, female wing; 7, male wing. C. nudipalpis Delfinado 3, female eye separation; 8, female wing; 9, male wing. 10, C. superfulvus Das Gupta cotype female wing. 11 C. radicitus Delfinado neotype male wing.

FIGURES 12 – 20. Female Culicoides (Avaritia) Imicola complex species. C. asiatica Bellis sp. n., 12, palpus; 15, mandibular teeth; 18, legs. C. brevitarsis Kieffer, 13, palpus; 16, mandibular teeth; 19, legs. C. nudipalpis Delfinado, 14, palpus; 17, mandibular teeth; 20, legs.

FIGURES 21 – 33. Culicoides (Avaritia) Imicola complex species. C. asiatica Bellis sp. n., 21, female antenna; 25, male antenna; 28, female tibial comb; 31, female spermathecae. C. brevitarsis Kieffer, 22, female antenna; 24, female antennal flagellomere 6; 26, male antenna; 29, female tibial comb; 32, female spermathecae. C. nudipalpis Delfinado, 23, female antenna; 27, male antenna; 30, female tibial comb; 33, female spermathecae.

FIGURES 43 – 45. Distribution of Culicoides (Avaritia) Imicola complex species. 43. C. asiatica Bellis sp. n. based on specimen data and published records (Lien et al. 1998; Henna et al. 1991, Wada et al. 1996; Yanase et al. 2011). 44. C. brevitarsis Kieffer based on specimen data, NAMP records and published records (Yu et al. 2005). 45. C. nudipalpis Delfinado based on specimen data and published records (Delfinado 1961; Wirth & Hubert 1989; Sukarsih et al. 1993; Lien et al. 1998).