Further Records of Biting Midges (Diptera: Ceratopogonidae) from Upper Cretaceous Burmese Amber (Myanmar)

Cretaceous Research 52 (2015) 556e561

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Cretaceous Research

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Further records of biting midges (Diptera: Ceratopogonidae) from Upper Cretaceous Burmese amber (Myanmar)

Ryszard Szadziewski a,*, Andrew Ross b, Wojciech Gi1ka a a Department of Invertebrate Zoology and Parasitology, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland b National Museum of Scotland, Department of Natural Sciences, Chambers St., Edinburgh EH1 1JF, United Kingdom article info abstract

Article history: A new biting midge Archiculicoides andersoni sp. nov. from Upper Cretaceous Burmese amber is described Received 20 January 2014 and illustrated. An unknown male of Leptoconops myanmaricus Szadziewski, 2004 is described and an Accepted in revised form 5 February 2014 undetermined female of the genus Archiaustroconops and Austroconops in the collection of National Available online 14 March 2014 Museums Scotland is reported. A key for the determination of 10 named species in 6 genera of biting midges reported from Burmese amber is also provided. Keywords: Ó 2014 Elsevier Ltd. All rights reserved. Diptera Ceratopogonidae Upper Cretaceous Burmese amber New species

1. Introduction was photographed by York in Ross and York (2000). Subsequently Johannsenomyia swinhoei Cockerell was redescribed and assigned The fossil record of Ceratopogonidae is one of the best known of all to the extinct genus Atriculicoides Remm, 1976 (Szadziewski, 2004). Diptera. There are presently 6243 named species with fossils repre- Rasnitsyn and Ross (2000) reported 12 biting midges (Cerato- senting 4.2% of these (Borkent, pers. comm.). The family is well pogonidae) among 1198 arthropods in 117 Burmese amber pieces documented from the Lower Cretaceous to the Neogene. From the preserved at The Natural History Museum, London. These biting Lower Cretaceous they are reported as inclusions from Lebanese midges (14) were studied by the senior author who described four ambers (Szadziewski, 1996; Borkent, 2000, 2001), Jordanian amber new species in two extant genera: Austroconops Wirth & Lee and (Szadziewski, 2000), Spanish ambers (Szadziewski & Arillo, 1998, Leptoconops Skuse (Szadziewski, 2004). 2003; Pérez-de la Fuente et al., 2011), Charentese amber from A collection of inclusions in Burmese amber purchased by the France (Choufani et al., 2011), and as a compression fossil from En- American Museum of Natural History, New York, includes 204 gland (Borkent et al., 2013). From the Upper Cretaceous, biting midges biting midges among 3012 arthropods (Grimaldi et al., 2002). are reported from Canadian, Siberian, New Jersey, French and Bur- Further specimens of biting midges in Burmese amber were pur- mese amber (Szadziewski, 1996, 2004; Szadziewski & Poinar, 2005; chased by George O. Poinar and deposited at Oregon State Uni- Borkent, 2000; Pérez-de la Fuente et al., 2011; Choufani et al., 2013). versity. This collection of 22 specimens was studied by Szadziewski The perceived age of Burmese amber or Burmite from Myanmar and Poinar (2005). has changed considerably in its history. It was first considered as Up to date nine named species of biting midges have been re- Miocene (Noetling, 1892), then Eocene (Cockerell, 1922), then more ported from Burmese amber in the genera Austroconopos (1), recently as Albian (Lower Cretaceous) in age (see Ross et al., 2010), Archiaustroconops (2), Leptoconops (4), Protoculicoides (1) and Atri- however it was recently dated as Cenomanian (Upper Cretaceous) culicoides (1) (Cockerell, 1919; Szadziewski, 2004; Szadziewski & by Shi et al. (2012). Poinar, 2005). Cockerell (1919) briefly described from Burmese amber the A small new collection of Burmese amber inclusions was pur- well-preserved male of Johannsenomyia swinhoei and this holotype chased by the National Museums Scotland (NMS) from Scott Anderson. Some of the specimens in this collection were figured by Ross et al. (2010) and Ross and Sheridan (2013). This collection * Corresponding author. E-mail addresses: [email protected] (R. Szadziewski), A.Ross@ contains four biting midge specimens, and they are the subjects of nms.ac.uk (A. Ross), [email protected] (W. Gi1ka). the present study. http://dx.doi.org/10.1016/j.cretres.2014.02.005 0195-6671/Ó 2014 Elsevier Ltd. All rights reserved. R. Szadziewski et al. / Cretaceous Research 52 (2015) 556e561 557

2. Materials and methods wing membrane became common in biting midges during the Upper Cretaceous period (Szadziewski, 1996, p. 82). Probably this wing Four biting midges (1 Archiculicoides,1Austroconops, 1 character evolved as an adaptation to changes of the physical Archiaustroconops and 1 Leptoconops) in four amber pieces from the properties of air in the Cretaceous atmosphere. National Museums Scotland (NMS) collection were examined. Spe- cial morphological terms and abbreviations used in the paper follow Subfamily: Leptoconopinae Noè, 1907 those explained by Szadziewski (1988,1996). The photographs were Genus: Archiaustroconops Szadziewski, 1996 taken using the LAS Montage multifocus with a Leica DM6000. Type species. Archiaustroconops ceratoformis Szadziewski, 1996

3. Systematic descriptions Lower Cretaceous (Lebanese amber, Alava and El Soplao ambers from Spain, compression fossil from England) and Upper Creta- Order: Diptera Linnaeus, 1758 ceous (Burmese amber). From Burmese amber, two species are Family: Ceratopogonidae Newman, 1834 described from males: A. gracilis Szadziewski et Poinar, 2005 and Basal lineage A. kotejai Szadziewski et Poinar, 2005. Genus: Archiculicoides Szadziewski, 1996 Archiaustroconops sp. indet. Type species. Archiculicodes schleei Szadziewski, 1996 Material examined. Single female. NMS, G.2010.20.43. Remark. The female now examined has no diagnostic characters Fossil genus reported as inclusions in Lower Cretaceous Leb- which allow the determination of the species. anese amber and now, for the first time, in Upper Cretaceous Bur- mese amber. Austroconops Wirth et Lee, 1958 Type species. Austroconops mcmillani Wirth et Lee, 1958 Archiculicoides andersoni sp. nov. Austroconops is an extant genus reported from the Lower 2013 Ceratopogonidae: Ross & Sheridan, p. 48, fig. 2, female. Cretaceous (Lebanese and Spanish ambers) and Upper Cretaceous (Burmese, French and Siberian ambers). From Burmese amber a Diagnosis. Female of the species is characteristic in having single species, Austroconops asiaticus Szadziewski, 2004, is known. sensilla coeloconica on first flagellomere, two distinct first radial Austroconops sp. indet. cells, rounded apex of terminal flagellomere and tarsal ratio of hind Material examined. Single female. NMS, G.2010.20.22. leg 1.4 times higher than that of fore leg. Male unknown. Remark. The examined female is devoid of diagnostic characters Description. Female. Body small, moderately robust with greatly which allow the determination of the species. elongated proboscis (Fig. 1A). Total length 0.95 mm. Eyes narrowly separated. Antenna with 13 flagellomeres; flagellum relatively long, Genus: Leptoconops Skuse, 1889 0.52 mm; proximal flagellomeres 2e8 subcylindrical, gradually Type species. Leptoconops stygius Skuse, 1889 increasing in length, distal 5 cylindrical; antennal ratio AR 1.0; first Leptoconops is an extant genus reported from Lower and Upper flagellomere with two groups of sensilla coeloconica, terminal Cretaceous and Paleogene ambers. Absent in Miocene Dominican flagellomere with evenly rounded apex (Fig. 1B). Proboscis greatly amber (Szadziewski & Grogan, 1994). From Burmese amber elongated, 1.4 times longer than height of eye (Fig. 1C). Palpus L. burmiticus Szadziewski, 2004, L. myanmaricus Szadziewski, 2004, slender, 5-segmented, length 0.193 mm; third palpal segment L. rossi Szadziewski, 2004, and L. subrossicus Szadziewski & Poinar, slender, cylindrical, 0.067 mm long, sensorium surficial (Fig. 1D). 2005 are reported. A male of L. myanmaricus is described below for Mandible barely visible, armed with small teeth. Wing without the first time. colour pattern, length measured from basal arculus 0.68 mm; wing Leptoconops myanmaricus Szadziewski, 2004 membrane without macrotrichia, microtrichia distinct; costa Leptoconops myanmaricus Szadziewski, 2004: 117 (female, Bur- reaching 0.8 wing length; both first radial cells well developed, mese amber). second one 1.5 times longer than first one; median veins petiolate Diagnosis. The only fossil species of Leptoconops with small tibial (Fig. 1E). Legs slender, unmodified. 4th tarsomeres cylindrical, spurs and low hind tarsal ratio (1.1e1.4), third palpal segment cy- claws similar on all legs, short, equal, simple. Tibial spur of hind leg lindrical and terminal palpomere rounded in both sexes, female small. TR(I) 2.7, TR(II) 2.6, TR(III) 1.9. TR of hind leg 1.4 times higher legs armed with toothed claws, and male genitalia with unique, than of fore leg (Fig. 1F, G). Genitalia barely visible. Cerci short. very long, apicolateral processes of tergite IX. Male unknown. Description. Male, well preserved (Fig. 2A). Body length 1.2 mm. Material examined. Female holotype. NMS, G.2010.20.24. In the Antenna with 13 flagellomeres, total length of flagellum 0.54 mm, same amber piece is one male of the subfamily Porricondylinae terminal flagellomere 0.190 mm long, 4.4 times longer than pre- (Diptera: Cecidomyiidae). The specimen is well preserved, complete. ceding one (Fig. 2B). Proboscis short, palpus 4-segmented. Third Etymology. The species name is dedicated to Mr Scott Anderson, palpal segment cylindrical, apex of terminal palpomere rounded who supplied the holotype. (Fig. 2C). Wing transparent (Fig. 2A), 0.82 mm long, costal vein Remarks. The new species, with two distinct groups of sensilla short, 0.28 mm, CR 0.34. Tarsal ratio TR (I) 2.21, TR(II) 2.00, TR(III) coeloconica on first flagellomere, is placed in the extinct genus 1.44 (Fig. 2D, E). Tarsal ratio of hind leg 1.5 times higher than that of Archiculicoides as diagnosed by Szadziewski (1996), Szadziewski and fore leg. Genitalia well visible (Fig. 2F, G). Tergite IX armed with two Poinar (2005) and Urbanek et al. (2014). The fossil genera Archicu- very long apicolateral processes (Fig. 2G, I). Gonocoxite with sub- licoides and Protoculicoides and extant genus Culicoides Latreille are apical ventral projection. Gonostylus armed at base with finger like morphologically very similar vertebrate blood feeders with the fe- and forked distally inner projection (Fig. 2H). male proboscis adapted for piercing skin. Archiculicoides and Culi- Material examined. Single male. NMS, G.2010.20.25(60). coides have sensilla coeloconica at least on first flagellomere while Remarks. Generally in the genus Leptoconops sexual dimorphism Protoculicoides is devoid of sensilla coeloconica. Culicoides has wing is distinct and the association of sexes based on morphology is membrane covered with macrotrichia while fossil genera have bare usually problematic. The male is considered to be conspecific with wings. The wing membrane of all known Lower Cretaceous biting the female of Leptoconops myanmaricus on the basis of similar midges have no macrotrichia. The presence of macrotrichia on the 558 R. Szadziewski et al. / Cretaceous Research 52 (2015) 556e561

Fig. 1. Archiculicoides andersoni sp. nov., holotype female. A, lateral habitus. B, antenna. C, head. D, palpus. E, wing. F, tarsomeres 1 and 2 of middle leg. G, tarsomeres 1 and 2 of hind leg. Scale bar: A ¼ 0.5 mm, BeG ¼ 0.1 mm. R. Szadziewski et al. / Cretaceous Research 52 (2015) 556e561 559

Fig. 2. Leptoconops myanmaricus Szadziewski, male. A, dorsal habitus. B, terminal ﬂagellomeres 11e13. C, palpus. D, tarsomeres 1 and 2 of middle leg. E, tarsomeres 1 and 2 of hind leg. F, G, dorsal aspect of genitalia. H, gonostyli. I, apicolateral processes of tergite IX. Scale bar: A ¼ 0.5 mm; B, D, E ¼ 0.1 mm; C, F, G, H, I ¼ 0.025 mm. 560 R. Szadziewski et al. / Cretaceous Research 52 (2015) 556e561 palps, low tarsal ratio of hind leg (1.1 female, 1.4 male), and small in moist soil in desert regions and in sand in coastal or inland tibial spurs (see key). beaches (Szadziewski, 2004). The predominance of Leptoconops may indicate that sea-shore habitats were near the amber pro- 4. Key to determination of genera and species of biting ducing trees. midges reported from Burmese amber

5. Concluding remarks Acknowledgements

The biting midge fauna preserved in Burmese amber is still We are indebted to Dr Elzbieta_ Sontag of the Museum of Amber poorly studied and includes ten named species in six genera so Inclusions (University of Gdansk) who prepared the preliminary far: Archiculicoides (1), Protoculicoides (1), Austroconops (1), version of photograph. Archiaustroconops (2), Leptoconops (4), Atriculicoides (1 species). Austroconops and Leptoconops are extant genera and were more widely distributed during the Cretaceous than now (Szadziewski, References 2008). It is worth mentioning that among the inclusions pre- Borkent, A., 2000. Biting midges (Ceratopogonidae: Diptera) from Lower Cretaceous served in Cretaceous and Paleogene ambers, only the extant Lebanese amber with a discussion of the diversity and patterns found in other genus Leptoconops is frequent in Burmese amber. Their larvae live ambers. In: Grimaldi, D. (Ed.), Studies in fossils in amber, with particular R. Szadziewski et al. / Cretaceous Research 52 (2015) 556e561 561

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