A revision of the cleptoparasitic bee genus Coelioxys (Hymenoptera: Megachilidae) from Australia

The Australian species of the genus Coelioxys Latreille are revised. Six species are recognized: Coelioxys albolineata Cockerell, 1905; Coelioxys froggatti Cockerell, 1911; Coelioxys reginae Cockerell, 1905; Coelioxys weinlandi Schulz, 1904 and two new species: Coelioxys julia sp. n. and Coelioxys tasmaniana sp. n. Three names are synonymized: Coelioxys biroi Friese, 1909 syn. n. and Coelioxys albolineata darwiniensis Cockerell, 1929 syn. n. under Coelioxys albolineata, and Coelioxys victoriae Rayment, 1935 syn. n. under Coelioxys froggatti. Species descriptions and redescriptions, illustrations, distribution maps, fl oral records and a key to both sexes of all species are provided. ZooBank Article LSID: 8E61B6E3-BA51-4583-A68F-37EDF62ECF8C


INTRODUCTION
The bee fauna from Australia is one of the most diverse and distinctive with a total of 1,651 species currently recognized and distributed among 64 genera (Australian Faunal Directory, 2006;Batley & Hogendoorn, 2009;Gonzalez et al., 2013).Most of this diversity is found within the family Colletidae which re presents 53.2% of all bee species in the country and also the most genera -32 (Australian Faunal Directory, 2006).Despite this highly diverse melissofauna, the parasitic bee fauna in Australia is poorly represented, with only two social parasites of the genus Inquilina Michener, 1961 and four genera of cleptoparasitic bees: Sphecodes Latreille, 1804 (Halictidae), Coelioxys Latreille, 1809 (Megachilidae), Nomada Scopoli, 1770 and Thyreus Panzer, 1806 (Apidae), the latter being the most species-rich, but still with only ten species (Australian Faunal Directory, 2006).Michener (1965) pointed out that the cuckoo bee fauna from Australia and South Pacifi c regions would be scarcer than in any major part of the world because most of the Australian bees are colletids, a family in which only fi ve parasitic species of Hylaeus (Nesoprosopis) Perkins, 1899 are known, all from Hawaii (Daly & Magnacca, 2003).
Considering that most Coelioxys spp.females parasitize nests of species of Megachile Latreille, 1802 (Michener, 2007), Cockerell (1905) mentioned F. Smith's observation about how singular it would be if Coelioxys was absent in Australia where Megachile is so abundant.This idea was also mentioned by Michener (1965) who stressed the surprising scarcity of Australian Coelioxys species compared there are two pairs of dorsal and ventral processes apically in the sixth tergum.
Six species of Coelioxys are recognized for Australia including two new ones: C. julia sp.n. and C. tasmaniana sp.n.Two species, C. julia sp.n. and C. weinlandi, belong to the subgenus Torridapis Pasteels, 1977.The other known species: C. albolineata, C. froggatti and C. reginae, have traditionally been considered to belong to the subgenus Coelioxys s. str.Latreille, 1809(Michener, 1965, 2007;Australian Faunal Directory, 2006;Ascher & Pickering, 2015).Nonetheless, an ongoing morphological phylogenetic analysis shows that C. (Coelioxys s. str.) is clearly paraphyletic and the three Australian species previously assigned to it as well as the new species C. tasmaniana sp.n. comprise two monophyletic subgenera that will be described (Rocha-Filho & Packer, in prep.).Hence, those four species are not placed under a subgeneric name in this paper.
Three species are placed in synonymy: C. biroi syn.n. and C. darwiniensis syn.n. under C. albolineata and C. victoriae syn.n. under C. froggatti (for details see species redescriptions section).A key to both sexes of the Australian species of Coelioxys is provided.Regarding the distribution records, C. tasmaniana is the only species recorded in Tasmania where it is endemic.Coelioxys froggatti is the only species known from Southern Australia and Victoria and most of its records are from southern areas of the latter state and Western Australia.Both C. albolineata and C. reginae occur predominantly along the Queensland coast, with some records from the northern parts of the Northern Territory and also in Papua New Guinea.The new species C. julia is only known from southern Queensland and northeastern New South Wales; Coelioxys weinlandi is recorded from the northern Queensland coast and also occur in Papua New Guinea.

Key to the Coelioxys species recorded in Australia
1 Compound eyes bare (Fig. 11B); F1 less than half as long as F2 (Fig. 9B); mesosoma mostly covered with black hairs (Fig. 11A); metanotum expanded basally, forming a deep sulcate area (Fig. 11C); axilla long, free part longer than attached part, conspicuously curved apically (Fig. 11C); wings dark, heavily infuscate with violet refl ections (Figs 9A,11A).Female: T6 and S6 greatly elongate, more than 2× longer than broad (Figs 9E, 11E); S5 greatly elongate towards apex, more than 1.5× longer than broad (Fig. 9A); lateral margins of S6 with fringe of short, plumose, brownish hairs (Figs 9E, 11E).Male: Hypostomal area lacking concavity (Figs 9I, 11G); gena unmodifi ed, not excavated along posterior margin of compound eye (Figs 9I,11G); S4 fl attened medially, forming two robust processes apically (Figs 9K,11J) erell, 1911 andC. peregrinata Cockerell, 1911 from the Solomon Islands, C. biroi Friese, 1909 from New Guinea and C. smithii Dalla Torre, 1896 from Indonesia.Since that article no major taxonomic study has been carried out for the genus Coelioxys in Australia.In the light of the above, the aim of this study is to provide a revision of the Australian species of Coelioxys, a key to separate the species of the genus, descriptions of two new species, redescriptions of the other species, three synonymies as well as fl oral records and distribution maps.

Taxonomic descriptions
The specimens studied belong to the following institutions: Australia -Australian Museum, Sydney (AMS); Australian National Insect Collection, Canberra (ANIC); Queensland Museum, Brisbane (QM); South Australian Museum, Adelaide (SAM); The terminology used for the species descriptions and redescriptions follows Mitchell (1973).All measurements are in millimeters (mm).The abbreviations used were F, T and S for fl agellomeres, metasomal terga and sterna, respectively.
The hidden sterna and genitalia of males were dissected and cleared in a 10% KOH solution, mounted on cavity slides with glycerine and then examined and photographed.Images were taken using a Visionary Digital BK Plus imaging system using a Canon EOS 40D digital SLR camera and processed with Adobe Photoshop©.Label data of type specimens were transcribed ipsis litteris.Different labels on the pin of the same specimen were cited between quotation marks (""); commas (,) were used to indicate breaks in text and a slash (/) to specify information on the underside of the label.Illegible words were mentioned as "[Illegible]" and misspelled words were followed by "[sic]" and the corrected spelling between brackets.

Floral, host and locality records
Data on fl oral, bee host and locality records were taken from specimen labels.Distribution maps were obtained with the assistance of the program DIVA-GIS 7.5 (DIVA-GIS 2015).
Colouration.Black except as follows: Antenna, mandible but apex, labrum, tegula, legs, sterna dark brown; wings subhyaline; veins brownish.In some specimens the mesoscutum, mesopleuron and legs are dark red.In some specimens with black colouration throughout the legs are brownish.
Surface sculpture.As in female except as follows: Postgradular areas of T2 with elliptical, transverse, shining, impunctate area laterally on each side but an elliptical puncture slightly larger than adjacent punctures; postgradular area of T3 indistinct, with elliptical, transverse, shining, impunctate area.T6 moderately densely punctate medially, punctures small, circular, sparsely punctate towards apex, punctures larger, elliptical.
Structure.Hypostomal concavity shallow, shorter than half length of compound eye.Gena deeply excavated along lower margin of eye, its length subequal to half eye length, both anterior and posterior margins of excavation linear, not enlarged anteriorly, excavation much longer than broad, its length about 4.5× longer than its width.Forecoxal apical spine-like projections short, fl at, rounded apically.In one male from Saltwater Creek, Qld, the posterior margin of mesoscutellum is not emarginate but it is upwardly oriented and produced medially.Spine-like processes of T5 pointed, separated from tergal surface apically.Basolateral processes of T6 long, acute, cylindrical; dorsal processes long, subacute apically, parallel one another; ventral processes acute apically, cylindrical, slightly divergent.T7 slightly tapering towards apex, rounded apically.Apical margin and apical rim of S4 entire.Apical margin of S5 entire, slightly fl attened medially.Apical rim of S5 entire.Gradulus of S5 semicircular.S6 membranous, gradulus indistinct, pregradular areas narrow, elongate, weakly sclerotized on inner margins, strongly sclerotized along outer margins, narrowly acute at base, apical half of pregradular area densely setose, less setose on outer margins, postgradular area transparent medially, broad at base, basal membranous lip rounded.S7 obsolescent, represented by two small sclerites.S8 base elongate, rounded apically, its apex slightly produced medially.Gonocoxa compressed laterally, with some long setae apically, longer than penis valve in length.
Comments.As stressed by Cockerell (1929) C. albolineata darwiniensis differs from C. albolineata only by the red colouration on mesoscutum, mesopleuron and legs.No discrepancies were found among specimens of both forms regarding both structural and sculptural characteristics.Additionally, some specimens of C. albolineata have brownish legs, an intermediate colour between the dark red observed in C. a. darwiniensis and the dark brown of C. albolineata.The two forms are sympatric in the northern parts of the Northern Territory and northern Queensland.However, the single example of C. albolineata from Western Australia is a male with red colouration collected near Mount Bruce, which is more than 2,700 km distant from Darwin, N.T., the closest locality considering the species' currently known distribution.
The syntypes of C. biroi were studied and no differences were found when compared to C. albolineata specimens and thus the former species was synonymized under the latter.When Friese (1909) described C. biroi based on a female he mentioned three specimens without indicating which was the holotype.From the three specimens he had, two had been collected in New Guinea by Biró (a female from "Simbang, Huon Golf" and a male from "Insel Thiar, Astrolabe Bai") and a female from "Key Inseln" collected by Kühn (apparently Kai Islands in Indonesia).However, in the ZMHB collection, there are six specimens identifi ed as C. biroi, three of them (one male labelled as "Type" and two females) from New Britain, Papua New Guinea (labelled as "Neu Pommern" and Neu Britannien" and identifi ed as C. biroi by Friese in 1910).Another female, labelled as from "Key Inseln" and identifi ed by Friese as C. biroi in 1909, seems to be the same species as the other three specimens from New Britain and might be one of the specimens Friese (1909) used for his description.The other two females were collected in 1921 in Buru, Indonesia and are different from the others mainly because of their dark wings and are not considered to belong to C. albolineata.In light of the above, it is stressed that two of the three specimens used in Friese's (1909) description were not located by the author and that the synonymy is based on the female from "Key Inseln" mentioned in the original description and on the three specimens from New Britain identifi ed by him as C. biroi in 1910.Additionally, in spite of the similarity between C. dispersa and C. albolineata the former is not being synonymized under the latter since in its male holotype the genal excavation is greatly elongate and linear, almost 6× longer than broad, whereas in the latter species it is about 4.5× longer than its width.Also the wings are weakly infuscate on the apical half; the apical fasciae on the terga are broadly interrupted medially and the T6 dorsal processes are rounded apically, rather than subacute apically in C. albolineata.
Host records.None.
Diagnosis.This species is very similar to C. reginae and C. tasmaniana.From the former, C. froggatti can be distinguished by the following list of characteristics: mesoscutum punctate to areolate; lateral surface of mesepisternum covered with appressed, plumose to scale-like hairs; posterior surface of mesoscutellum covered with subappressed, plumose to scale-like hairs; apical fasciae on terga complete.In females the compound eye is distinctly convex basally and the lateral margins of S6 are conspicuously angled subapically.In males the T6 dorsal processes are elongate, narrow and rounded apically and the S4 apical margin and apical rim medially in lateral view are not angled, both surfaces in the same level.The main difference between C. froggatti and C. tasmaniana is the hairs on head, mesoscutum and mesepisternum which are appressed in the former species but are distinctly suberect in the second.
Pubescence.White, appressed/subappressed on: Paraocular area, supraclypeal area, clypeus (sparse medially), inconspicuous fringe on apical margin of clypeus, gena, mandible basally, lateral margins of mesoscutum, mesepisternum, legs, basal fascia on T1, apical fascia on sterna (interrupted medially).Ocular hairs whitish and short (about 0.07 mm).Scattered, suberect, slender, whitish setae on paraocular area and supraclypeal area.Upper paraocular area hairs long, white distinct from those of adjacent regions, oriented mesad, apices of some from each side almost meeting medially.Scattered, slender, suberect, long, golden setae on dorsal surface of mandible.Slender, suberect, whitish setae arising from punctures on vertex and mesoscutum.Thick, yellow setae on tarsi.Appressed, elongate, plumose to scale-like, white hairs on vertex posteriorly, transverse fascia anteriorly on mesoscutum, two large, elliptical sublateral spots between mesoscutellum and mesoscutum, laterally on subaxilla, mesopleuron, ventral surface of mesepisternum, posterior surface of mesoscutellum, medially on metanotum, lateral bands on T1, on apical fasciae of T1-T5 and elliptical, dense tufts on lateral margins of T6.In some females the transverse fascia anteriorly on mesoscutum is absent or inconspicuous, formed by a few, sparse hairs.The spots of appressed hairs on mesoscutellum vary in size, being larger and more circular in some specimens and narrower in others.Erect, long, thin pale hairs on metanotum.Postgradular area of S6 except subapical area covered with minute, very short, suberect pale setae.
Colouration.As in female except as follows: T1 black throughout.
Pubescence.As in female except as follows: Face densely covered with appressed, long, white hairs; hypostomal concavity covered with very short, white hairs, longer hairs on anterior margins; genal excavation densely covered with appressed, plumose white hairs.Transverse fascia anteriorly on mesoscutum inconspicuous, formed by a small spot of appressed hairs medially.Gradular grooves of T5-T6 conspicuously fasciate with appressed, plumose, white hairs, gradular groove of T4 not fasciate.Long, suberect, pale setae arising from punctures on T6.
Structure.Hypostomal concavity shallow, shorter than half length of compound eye.Gena deeply excavated along lower margin of eye, its length subequal to half eye length, excavation not linear, its posterior margin greatly enlarged anteriorly, excavation longer than broad, its length about 3× longer than its width.Forecoxal apical spine-like projections short, fl at, rounded apically.Spine-like processes of T5 robust, separated from tergal surface apically.Basolateral processes of T6 long, acute, fl attened laterally; dorsal processes elongate, rounded apically, slightly divergent; ventral processes acute apically, cylindrical, slightly divergent.T7 rounded apically.Apical margin and apical rim of S4 entire, in the same level, not angled in lateral view.Apical margin of S5 entire, slightly fl attened medially.Apical rim of S5 entire.Gradulus of S5 angulate towards base, semicircular.S6 membranous, gradulus indistinct, pregradular areas narrow, elongate, weakly sclerotized on inner margins, strongly sclerotized along outer margins, narrowly acute at base, apical half of pregradular area densely setose, less setose on outer margins, postgradular area transparent medially, broad at base, basal membranous lip rounded.S7 obsolescent, represented by two small sclerites.S8 base elongate, rounded apically, its apex entire, rounded.Gonocoxa compressed laterally, with some long setae apically, longer than penis valve in length.
Comments.The name C. victoriae was synonymized with C. froggatti because both female holotypes are indistinguishable.Host records.None.
Diagnosis.This is the only Australian species in which the S6 of the female is conspicuously notched subapically and the S4 apical margin in the male is angled to the apical rim.In spite of the resemblance of C. reginae to C. froggatti and C. tasmaniana the fi rst can be differentiated from the other two by the apical fasciae on terga interrupted medially, the apical fasciae on sterna weakened medially, the forewing weakly infuscate on the apical half and the mesoscutal sculpturing never areolate.In females of C. reginae the compound eye is not convex towards the base (close to mandible; seen in lateral view) as in both C. froggatti and C. tasmaniana and S6 is conspicuously notched subapically contrasting to the angled lateral margins subapically found in the other two species.In males the T6 dorsal processes are short, broad, broadly rounded apically (elongate and narrow in C. froggatti and C. tasmaniana) and the S4 apical margin is elevated, angled to apical rim in lateral view (both surfaces not angled in the other two species).
Surface sculpture.As in female except as follows: Postgradular areas of T2 indistinct, with elliptical, transverse, shining area with few sparse punctures laterally on each side, on T3 nearly impunctate.T6 moderately densely punctate medially, punctures small, circular, sparsely punctate towards apex, punctures larger, elliptical.
Structure.Hypostomal concavity shallow, shorter than half length of compound eye.Gena deeply excavated along lower margin of eye, its length subequal to half eye length, excavation not linear, its posterior margin greatly enlarged anteriorly, excavation longer than broad, its length about 3.5× longer than its width.Forecoxal apical spine-like projections long, fl at, subacute apically.Spine-like processes of T5 robust, separated from tergal surface apically.Basolateral processes of T6 long, acute, fl attened laterally, divergent; dorsal processes short, broad, rounded apically, divergent; ventral processes acute apically, cylindrical, slightly divergent.In some males the T6 dorsal processes can be slightly slanting.T7 slightly tapering towards apex, rounded apically.Apical margin and apical rim of S4 entire, apical margin elevated, forming an angle to apical rim.Apical margin of S5 entire, slightly fl attened medially.Apical rim of S5 entire.Gradulus of S5 semicircular.S6 membranous, gradulus indistinct, pregradular areas narrow, elongate, weakly sclerotized on inner margins, strongly sclerotized along outer margins, narrowly acute at base, apical half of pregradular area copiously and densely setose, less setose on outer margins, postgradular area transparent medially, broad at base, basal membranous lip rounded.S7 obsolescent, represented by two small sclerites.S8 base elongate, subacute apically, its apex entire, rounded.Gonocoxa compressed laterally, with some long setae apically, longer than penis valve in length.
Comments.Both C. reginae and C. albolineata have similar distribution patterns throughout northern region of Northern Territory and along northern Queensland coast.Nonetheless, the former is also found in southern Queensland inland and New South Wales but is absent in Western Australia in contrast to the range of C. albolineata.Host records.None.
Diagnosis.Coelioxys tasmaniana is very similar to C. froggatti.They share some distinctive characters not found in the other Australian species as in females the compound eye is convex basally and the lateral margins of S6 angled to subangled (but inconspicuously notched in the female holotype of C. tasmaniana).Also in males the dorsal processes of T6 are elongate and the apical margin of S4 is not elevated.These two species can be distinguished by the suberect, long, thin hairs on the face, mesoscutum and mesepisternum observed in C. tasmaniana that contrasts to the appressed, plumose hairs of C. froggatti.Additionally, the posterior surface of the mesoscutellum and the metanotum medially in C. froggatti are covered with scale-like, appressed hairs whereas in C. tasmaniana both are covered with elongate, suberect hairs.Description, female.Measurements (holotype).Body length: 6.72 mm; forewing length: 3.76 mm; head width: 1.88 mm.
Surface sculpture.As in female except as follows: Postgradular areas of T2-T3 indistinct, with a very few small punctures laterally on each side.T6 moderately densely punctate medially, punctures small, circular, sparsely punctate towards apex, punctures larger, elliptical.
Structure.Hypostomal concavity shallow, shorter than half length of compound eye.Gena deeply excavated along lower margin of eye, its length longer than half eye length, excavation not linear, its posterior margin greatly enlarged anteriorly, excavation longer than broad, its length about 3× longer than its width.Forecoxal apical spine-like projections short, fl at, acute apically.Spine-like processes of T5 robust, separated from tergal surface apically.Basolateral processes of T6 long, rounded apically, fl attened laterally; dorsal processes elongate, rounded apically, slightly divergent; ventral processes acute apically, cylindrical, slightly divergent.T7 rounded apically.Apical margin and apical rim of S4 entire, in the same level, not angled in lateral view.Apical margin of S5 entire, slightly fl attened medially.Apical rim of S5 entire.Comments.This is the only species recorded from Tasmania and its distribution is restricted to this island.As only two males were available the terminalia were not dissected.
Etymology.The epithet "tasmaniana" refers to distributional range of this species that is restricted to that island.
Floral records.None.Host records.None.
Diagnosis.Among Australian Coelioxys this new species and C. weinlandi are the only ones with bare eyes and heavily infuscate wings.Coelioxys julia is very similar to C. weinlandi from which it can be differentiated by the black pubescence on the vertexal and occipital areas; mesoscutum sparsely punctate, with polished interspaces between punctures; lack of a dorsal carina medially on posterior margin of mesoscutum and white pubescence on ventral surface of mesepisternum.Females of C. julia can be distinguished by the apical margin of clypeus simple; lack of sparse appressed hairs sublaterally on S2-S4 and evanescent lateral carinae on T6 subapically.Males can be separated from those of C. weinlandi by the inconspicuously elevated processes of S4 apical margin; long, acute teeth basally on T6 and lack of apicolateral white bands on the metasomal terga.
Colouration.Black except as follows: Antenna dark brown, legs blackish; tarsal claws light brown; wings heavily infuscate with dark blue to violet refl ections; veins dark brown.
Colouration.As in female.Pubescence.As in female except as follows: Clypeus fully covered with white subappressed hairs, more sparse medially.White, appressed hairs on half apex of S4-S5 medially.Apical margins of terga laterally lacking bands of appressed white hairs.Postgradular grooves of T2-T6 not fasciate.
Surface sculpture.As in female except as follows: Postgradular areas of T2-T3 unmodifi ed, lacking fovea or punctate areas sublaterally.T6 sparsely punctate, interspaces between punctures polished, smooth and larger than puncture diameter.
Structure.Ocelloccipital distance subequal to ocellocular distance.Hypostomal area lacking concavity.Forecoxal apical spine-like projections short, subacute apically, triangular.Apex of T5 lacking spine-like processes.Basolateral processes of T6 long, triangular, fl at, acute apically; dorsal processes short, slanting, broadly rounded apically; ventral processes subacute apically, cylindrical.Half apex of S4 fl attened medially, apex forming two inconspicuously elevated processes shorter than the distance that separates them.Half apex of S5 fl attened medially, not forming processes.
Comments.Coelioxys julia is only known from southeastern Queensland and northeastern New South Wales.As only the male paratype was available for this study, the terminalia were not dissected.
Etymology.The specifi c epithet is a noun in apposition and is named in honour of the former Prime Minister of Australia Julia Gillard for her commitment and engagement with the environmental cause in that country.
Floral records.None.Host records.None.
Geographical distribution.Australia (New South Wales, Queensland) (Fig. 10).Diagnosis.Coelioxys weinlandi and C. julia are the only species that belong to the subgenus Torridapis recorded in Australia.Both are readily recognized by their large size, often exceeding 7.5 mm; bare eyes; heavily infuscate wings with violet refl ections and dark pubescence mainly on the mesosoma.In spite of their similarity, C. weinlandi is characterized by the dense white pubescence posteriorly on the vertex and on the occipital area; sharp dorsal carina medially on the posterior margin of the mesoscutellum; rugose, coarse sculpture of the mesoscutum, lacking polished interspaces and the dark brown pubescence on the ventral surface of the mesepisternum.In females the apical margin of the clypeus is produced medially; apical white fasciae on the metasomal terga are complete and distinct and the lateral carinae on T6 are not evanescent and form an elongate U-shaped carina.Males of C. weinlandi are differentiated from those of C. julia by the conspicuously elevated processes of S4 apical margin; presence of white tergal bands laterally and short lateral teeth basally on T6.
Colouration.As in female.Pubescence.As in female except as follows: Clypeus fully covered with white subappressed hairs, more sparse medially.White, appressed hairs forming large bands laterally on apical margins on T1-T5; on postgradular grooves of T2-T6; half base of S4 medially.Apex of pregradular area of S6 laterally and gonocoxite apically densely covered with suberect, plumose, brown hairs.
Surface sculpture.As in female except as follows: Postgradular areas of T2-T3 lacking fovea or punctate areas sublaterally.T6 moderately densely punctate.
Comments.This species is known from northern Queensland in Australia and from Papua New Guinea while C. julia is only known from southeastern Queensland.Both the female syntype of C. albiceps and female holotype of C. weinlandi were compared and they share the same diagnostic characteristics and cannot be differentiated.
Floral records.None.Host records.Friese (1909) mentioned that according to Biró C. weinlandi (cited as C. albiceps) is a parasite of Ctenoplectra chalybea Smith (Apidae).However, Michener (1965) emphasized this record was certainly an error and the geographic ranges of the two species do not overlap.