Four new species of Gasteruption Latreille from NW China, with an illustrated key to the species from Palaearctic China (Hymenoptera, Gasteruptiidae)

Abstract Four new species of the genus Gasteruption Latreille, 1796 (Hymenoptera: Evanioidea: Gasteruptiidae: Gasteruptiinae) are reported from NW China: three from Shaanxi province and one from Ningxia province. The new species (Gasteruption bicoloratum Tan & van Achterberg, sp. n., Gasteruption huangshii Tan & van Achterberg, sp. n., Gasteruption pannuceum Tan & van Achterberg, sp. n., and Gasteruption shengi Tan & van Achterberg, sp. n.) and three newly recorded species (Gasteruption sinepunctatum Zhao, van Achterberg & Xu, 2012, Gasteruption boreale (Thomson, 1883) and Gasteruption oshimense Watanabe, 1924) are keyed and fully illustrated. In total, seven species are known from Shaanxi province, which is approximately half of the expected number. The East Palaearctic specimens provisionally identified as Gasteruption tournieri Schletterer, 1885, by Zhao et al. (2012) are included under Gasteruption oshimense Watanabe, 1924.


Introduction
The family Gasteruptiidae is a small group of wasps comprising about 500 described species in two subfamilies, Gasteruptiinae (four genera) (Macedo 2009(Macedo , 2011Zhao et al. 2012) and Hyptiogastrinae (two genera) (Jennings and Austin 2002). Gasteruptiidae are easily distinguished from the other apocritan hymenopterans by the elongated "neck" (propleuron), the swollen hind tibiae, and the highly attached and slender metasoma. Adults are free-living insects normally feeding on nectar from flowers with easily accessible nectar (especially families Apiaceae, Asteraceae and Euphorbiaceae), but likely at least some Gasteruption species feed on both nectar and pollen (Jennings and Austin 2004). Gasteruptiidae are also known by their hovering inspection flight in front of bee nests ( van Achterberg 2013). The larvae feed on the larval food of solitary bees, after consuming the egg or larva of the bee (Malyshev 1966). They select bees of the subfamilies Apinae, Colletinae and Megachilinae nesting in stems or in wood, and less often in clay banks or other vertical soil substrates (Malyshev 1965;Zhao et al. 2012; van Achterberg 2013); as far as known, bees nesting in horizontal soil substrates are far less attacked. However, in Australia members of the Hyptiogastrinae do attend bee nests in flat ground (Houston 1987). There is only indirect evidence that Gasteruptiinae may attack wasp nests, especially of Crabronidae, Sphecidae and solitary Vespidae (Eumeninae) (Crosskey 1951;Gauld 2006;Jennings and Austin 1997a, 1997b, 2004. Metamorphosis takes place inside the host's nest where the gasteruptiid pupa hibernates until the next spring or summer (Malyshev 1968;He 2004;Jennings and Austin 2004). All known gasteruptiids from the Palaearctic Region belong to the subfamily Gasteruptiinae and to the genus Gasteruption Latreille, 1796. For identification the revision of the Chinese species (Zhao et al. 2012) and the yet unpublished revision of the East Palaearctic species ( van Achterberg, in prep.) were used. According to Zhao et al. (2012) two species (G. angulatum Zhao, Xu, 2012 andG. japonicum Cameron, 1888) are known from the NW Chinese province Shaanxi, which is 7% of the total of 28 species reported from China. Italy (about as varied in natural habitats as Shaanxi) is 50% larger than Shaanxi but has 20 species reported, which is about 60% of the total species known from Europe. In this paper we report five additional species, and from the comparison with Italy it may be deduced these seven are about half of the number to be expected.

Material and methods
The specimens were mainly collected by hand net or sweep netting, rarely in Malaise traps during 2015. Specimens from Shaanxi were directly stored in 70% ethanol, prepared using the AXA method ( van Achterberg 2009;van Achterberg et al. 2010) and glued on card points; other specimens were directly pinned. Observations and descriptions were made with an Olympus SZX11 stereomicroscope and fluorescent lamps. Photographic images were made either with a Keyence VHX-5000 digital microscope or with an Olympus motorized stereomicroscope SZX12 and processed with Adobe Photoshop CS5, mostly to adjust the size and background.
For comparison of head shapes it is essential that the middle of the vertex is in plane of objective of binocular microscope. For the other terminology, see Zhao et al. (2012) and van Achterberg (1988). Measurements are performed as indicated in Fig. A-B and in van Achterberg (1988). Additional non-exclusive characters in the key are between square brackets. The association of males with females is based on similarity. In the few cases in which no males were available, distinctive, and probably non-sexual, characters of the female were tentatively used for inclusion in the key. A new provincial record is indicated by an asterisk. The following abbreviations are used for the depositories: Malar space in anterior view 0.5-0.6 times length of pedicellus and 0.4-0.6 times basal width of mandible and mandibular condylus distinctly below lower level of eyes (a); in lateral view condylar incision of malar space remains far removed from eye (b); ovipositor sheath 0.4-0.9 times as long as hind tibia (c); first discal cell of fore wing usually suddenly narrowed (d  24 Pale apical part of ovipositor sheath 3.0-3.5 times as long as hind basitarsus (a); vertex shiny and largely smooth or finely punctulate (b); fourth antennal segment 1.7-2.3 times as long as third antennal segment (c); mesoscutum more or less coarsely spaced punctate or punctate-rugose medio-posteriorly (d  (2012) to G. oriplanum Kieffer, 1911 (but the malar space is shorter in the new species and oblique in anterior view, not subparallel-sided below eyes in anterior view as in G. oriplanum and the mandibles are paler) or to G. assectator (Linnaeus, 1758). The pale fifth sternite of the female, the strongly narrowed head in dorsal view, the shorter ovipositor sheath (about 0.6 times hind tibia vs 0.9-1.3 times in G. assectator) and the yellowish mandible separate it from G. assectator. The new species is close to G. flavimarginatum , but it has a slightly longer malar space (short in G. flavimarginatum), the hind basitarsus slender and dorsally dark brown (rather robust and at least partly ivory dorsally) and the mesoscutum finely sculptured (coarser sculptured). The male differs by having the apex of the paramere dark brown, which is yellowish brown in G. flavimarginatum.
Description. Holotype, female, length of body 9.9 mm, of fore wing 4.9 mm.
Head. Vertex and frons with satin sheen, finely coriaceous, moderately convex and without a depression medio-posteriorly; head directly contracted behind eyes in dorsal view and temples nearly straight (Fig. 14); temple 0.9 times as long as eye in dorsal view; fourth antennal segment 1.2 times as long as third segment and 0.7 times as long as second and third segments combined, fifth antennal segment as long as third segment, third antennal segment 1.6 times as long as second segment (Fig. 8); occipital carina narrow and non-lamelliform medio-dorsally (Fig. 8); OOL 1.3 times as long as diameter of posterior ocellus; face wide, 2.8 times as broad as high, 2.4 times as wide as eye in frontal view (Fig. 13); malar space somewhat protruding below lower level of eyes (Fig. 13), its minimum width 0.4 times as long as second antennal segment and 0.35 times basal width of mandible and area behind incision nearly square (Fig. 8); clypeus only medio-ventrally shallowly depressed (Fig. 13); eye with numerous short setae.
Wings. First discal cell parallel-sided and with outer posterior corner rounded, and with vein 3-CU1 near its apical third (Fig. 11).
Legs. Hind coxa finely granulate-coriaceous; length of hind femur, tibia and basitarsus 3.9, 3.6 and 4.6 times their width, respectively; hind tibia strongly inflated (Fig.  15); middle tarsus 1.1 times as long as middle tibia; middle femur subparallel-sided and slimmer than fore femur. Metasoma. Ovipositor sheath 1.2 mm, 0.1 times as long as body, 0.2 times as long as metasoma and 0.6 times as long as hind tibia; ovipositor sheath with dense cover of fine brownish and adpressed setae, its apical half slender; hypopygium shallowly emarginate medio-posteriorly.
Variation. Body length of ♀ 8.7-10.3 mm, of ♂ 8.2-9.9 mm; length of ovipositor sheath 0.6-0.7 times hind tibia; minimum width of malar space 0.3-0.4 times as long as second antennal segment; tibiae and tarsi more or less yellowish brown ventrally; apical antennal segment more or less obliquely depressed.

Gasteruption boreale (Thomson, 1883) Figs 23-32
Foenus borealis Thomson, 1883: 849;Hedicke 1939: 7;Hedqvist 1973: 181, 182 (invalid lectotype designation); Wall 1994: 148. Synonymized with G. assectator (Linnaeus) by Schletterer (1889) (Fig. 30), elongate, about as wide as long; occipital carina indistinct medio-dorsally; frons with satin sheen; mesoscutum rather weakly rugulosecoriaceous or chagreened, similar as vertex (Fig. 24) and with satin sheen, in front of scutellum rather rugose (Fig. 26); mesosoma and head silvery pilose; mesosoma with a satin sheen, quite distinct from the rather fatty gloss present in G. assectator s.s.; whitish pubescence of eye of female (Fig. 29) mostly distinctly longer and denser than of G. assectator s.s.; antenna slightly shorter than in G. assectator s.s. with sixth segment about 1.5 times longer than wide and subapical segment about 1.2 times longer than wide; only apical half of hind coxa weakly striate dorsally; hind tibia and basitarsus with white or ivory ring (Fig. 27); metasoma mainly black with orange lateral patches on tergites 2-4, which might be partially reduced (Fig. 23); inner sides of tibiae often red brown to orange with white or yellow basal patch indistinct on fore and middle tibiae; ovipositor sheath black or brown, 0.7-1.0 times as long as hind tibia, its apical half entirely with stout, rather scarce black bristles angled backwards at about 45° (Fig.  32). The male is difficult to separate from males of G. assectator s.s. and identification is not always possible with certainty. In most cases males of G. boreale have a slightly more elongate and subparallel-sided head in dorsal view, a less sculptured mesoscutum and a more or less enlarged malar space.

Gasteruption huangshii
Description. Holotype, female, length of body 12.5 mm, of fore wing 6.0 mm. Head. Vertex and frons with satin sheen, finely and densely punctulate (but vertex with some fine additional punctures: Fig. 40), moderately convex and without a depression medio-posteriorly; head trapezoid and gradually narrowed behind eyes in dorsal view and temples convex (Fig. 40); temple 0.7 times as long as eye in dorsal view; fourth antennal segment 1.5 times as long as third segment and 0.9 times as long as second and third segments combined, fifth antennal segment 1.2 times as long as third segment (Fig. 33), third antennal segment 1.4 times as long as second segment; occipital carina narrow and narrowly lamelliform medio-dorsally (Figs 34, 40); OOL 1.3 times as long as diameter of posterior ocellus; face 2.7 times wider than high, 2.4 times wider than eye in anterior view (Fig. 39); minimum width of malar space 0.3 times as long as second antennal segment (Fig. 34); clypeus rather flat and with small round emargination medio-ventrally; eye glabrous.
Wings. First discal cell parallel-sided and with outer posterior corner rounded, and with vein 3-CU1 near apical third (Fig. 37).
Legs. Hind coxa very finely coriaceous-punctulate; length of hind femur, tibia and basitarsus 2.7, 3.5 and 4.1 times their width, respectively; middle tarsus 1.1 times as long as middle tibia; middle femur subparallel-sided and slimmer than distinctly widened fore femur.
Metasoma. Ovipositor sheath 15.3 mm, 1.2 times longer than body, 1.7 times as long as metasoma and 7.5 times as long as hind tibia, ivory apical part of sheath 1.8 times as long as hind basitarsus; apical half of hypopygium incised (Fig. 38).
Colour. Black; mandible dark brown with middle part brown; fore femur apically, fore and middle tibiae basally and apically, and hind tibial spurs yellowish brown; hind tibia ventro-basally ivory; tegulae and remainder of legs mainly dark brown; pterostigma dark brown; wing membrane subhyaline.
Male. Similar to female, but head behind eye slightly more contracted in dorsal view and somewhat shorter (Fig. 47); third antennal segment as long as second segment, fourth antennal segment 2.5-2.9 times as long as third segment and 1.3-1.5 times as long as second and third segments combined, fifth antennal segment 2.6-2.9 times as long as third segment (Fig. 46); mouthparts ivory; paramere densely whitish setose and its apex brownish yellow (Fig. 48).
Variation. Body length of male 8.7-9.9 mm; sculpture of mesosoma of male very fine and only slightly coarser coriaceous than of female.  Distribution. China (Shaanxi). Biology. Unknown, but the new species was collected together with a Hylaeus sp. Etymology. Named after Huang Shi Gong (supposed teacher of the early Han general Zhang Liang), because the specimens were collected outside the hall with Huang Shi Gong's statue at the Zhang Liang Temple.

Gasteruption japonicum Cameron, 1888 Figs 49-57
Gasteruption japonicum Cameron, 1888: 134;Zhao et al. 2012: 58-61. Gasteruption sinense var. minus Kieffer, 1924Zhao et al. 2012: 58 (synonymized with G. japonicum , 1913, is obviously different from the paralectotype male (e.g. head not emarginate medioposteriorly and more narrowed, narrower occipital carina and different sculpture of mesoscutum) and is very similar to G. japonicum. The differences as indicated in the key could be part of gradual variation and after examination of more Japanese material its status may need reconsideration.   Watanabe, 1934 Figs 58-67 Gasteruption oshimensis Watanabe, 1934: 283-284. Gasteruption tournieri;Zhao et al. 2012: 103-108. Material. 2♀ (NWUX), China: Shaanxi, Zhashui, Huanghualing., N33.76° E108. 85°, 23.vii.2015, c 1577 N33°39'29" E107°48'25", 29.v.-19.vi.2016, c 1710 Notes. The East Palaearctic specimens provisionally identified as G. tournieri Schletterer, 1885, by Zhao et al. (2012 are included here under G. oshimense Watanabe. The different shape of the head was noticed before, but also the hind tibia and hind basitarsus are slimmer and the sculpture of the mesoscutum is less developed. Most likely it concerns a separate species and because a valid name is available, this name (correctly spelled as G. oshimense) is used here. Especially the size of the males is very variable, e.g. length of body is 5.3-8.7 mm in the series from Langoa collected at the same spot and within one hour.    N34°03' E108°09', c 700 m, 10.vi.2015, 24.v.2015 Comparative diagnosis. Runs in Zhao et al. (2012) either to G. varipes (Westwood, 1851) (if the pale apical part of the ovipositor sheath is considered to be minor) or to G. sinarum Kieffer, 1911 (if the pale part is considered to be intermediate; Fig.  77). The new species differs from G. varipes by having the mesopleuron black and finely sculptured (orange brown and coarsely vermiculate-reticulate (rarely only weakly so)), the mesoscutum slender and finely rugulose (robust and coarsely rugose), the propodeum mainly coriaceous (coarsely vermiculate-rugose), a shorter ovipositor sheath (3 times hind tibia vs 5 times) and the mandible brownish yellow (blackish). The new species differs from G. sinarum by having a shorter ovipositor sheath (3.2 times hind tibia vs 4.8-6.0 times in G. sinarum), the mesoscutum without coarse punctures (present), the vertex shiny and largely smooth (with satin sheen and punctulate in G. sinarum) and the vertex distinctly convex (less so in G. sinarum). It shares with G. parvicollarium Enderlein, 1913, the convex vertex, but the new species has a longer ovipositor sheath (3.1 times hind tibia vs 1.2-1.7 times in G. parvicollarium), the mesoscutum transversely wrinkled (mainly coriaceous) and eyes more conspicuously setose.
Head. Vertex and frons shiny and very finely punctulate, nearly smooth (Fig. 75), distinctly convex (Fig. 69) and without a depression medio-posteriorly; head trapezoid and directly narrowed behind eyes in dorsal view (Fig. 75); temple 0.7 times as long as eye in dorsal view; fourth antennal segment 1.1 times as long as third segment and 0.6 times as long as second and third segments combined, fifth antennal segment 1.2 times as long as third segment, third antennal segment 1.4 times as long as second segment; occipital carina narrow and non-lamelliform medio-dorsally (Figs 69, 75); OOL 1.5 times as long as diameter of posterior ocellus; face 3.5 times wider than high, twice wider than eye in anterior view (Fig. 74); minimum width of malar space 0.2 times as long as second antennal segment (Fig. 69); clypeus rather flat, slightly depressed ventrally and shallowly emarginate medio-ventrally; eye densely setose (Fig. 74).
Metasoma. Ovipositor sheath 8.5 mm, 0.8 times longer than body, 1.1 times as long as metasoma and 3.2 times as long as hind tibia, ivory apical part of sheath 0.3 times as long as hind basitarsus; apical 0.3 of hypopygium incised (Fig. 73).
Colour. Black; mandible brownish yellow and basally slightly darkened; apical antennal segment, apex of ovipositor sheath, fore and middle tibiae basally and hind tibia ventro-basally ivory or pale brown; penultimate antennal segment brown; tegulae, pterostigma, remainder of legs and antenna, hind tibial spurs and remainder of legs mainly dark brown or blackish; wing membrane subhyaline.
Male. Unknown. Distribution. China (Shaanxi). Biology. Unknown. Etymology. Named after the rugulose ("wrinkled") sculpture of the middle lobe of the mesoscutum: "pannuceus" is Latin for "wrinkled". Comparative diagnosis. Runs in Zhao et al. (2012) to G. dimidiatum Semenov, 1892, because of the emarginate head, the long and black ovipositor sheath, punctate mesoscutum and the finely sculptured propodeum. The new species differs from G. dimidiatum by having the head not prolonged below eyes in anterior view and malar space 0.2-0.3 times as long as second antennal segment (head shortly prolonged below eyes in G. dimidiatum; fig. 107 in Zhao et al. 2012, malar space 0.4 times as long as second antennal segment), first metasomal tergite black (orange or yellowish brown), basal half of hind coxa only coriaceous (transversely rugulose), apex of ovipositor sheath black (narrowly ivory), mesoscutum rather finely punctate (somewhat coarser punctate) and slightly wider hind tibia (slightly narrower). Males may be confused with G. sinarum Kieffer, 1911, the latter species has the hind coxa distinctly transversely rugose, the hind tibia is slim and the mesoscutum is more or less rugulose.
Description. Holotype, female, length of body 13.1 mm, of fore wing 5.9 mm.
Head. Vertex and frons with satin sheen and very finely punctulate, but vertex posteriorly superficially coriaceous (Fig. 86), distinctly convex (Fig. 80) and without a depression medio-posteriorly; frons densely silvery setose anteriorly; head trapezoid and gradually narrowed behind eyes in dorsal view (Fig. 86); temple 0.7 times as long as eye in dorsal view; fourth antennal segment 1.4 times as long as third segment and 0.9 times as long as second and third segments combined, fifth antennal segment 1.1 times as long as third segment, third antennal segment 1.8 times as long as second segment; occipital carina narrow and hardly lamelliform medio-dorsally (Figs 80, 86); OOL 1.4 times as long as diameter of posterior ocellus; face 3 times wider than high, 2.2 times wider than eye in anterior view (Fig.  85); minimum width of malar space 0.2 times as long as second antennal segment (Fig. 80); clypeus rather flat, slightly depressed ventrally and distinctly emarginate medio-ventrally (Fig. 85); eye largely glabrous; head shallowly U-shaped emarginate posteriorly (Fig. 86).
Mesosoma. Length of mesosoma twice its height; propleuron rather robust and 0.8 times as long as mesoscutum in front of tegulae; pronotal side mainly superficially coriaceous, with grooves crenulate and largely densely silvery setose, with small acute tooth antero-ventrally (Fig. 80); antesternal carina narrow and non-lamelliform; mesopleuron coriaceous and largely densely silvery setose; mesosternal sulcus rather wide and crenulate; mesoscutum and scutellum with satin sheen, mesoscutum rather coarsely punctate but interspace mostly wider than diameter of punctures, interspaces superficially coriaceous, but middle lobe medio-posteriorly with few rugae (Fig. 82); scutellum mainly superficially coriaceous and with few small punctures; propodeum mainly coriaceous but medially with transverse crenulation connected to smooth median area. Wings. First discal cell parallel-sided and with outer posterior corner rounded and with vein 3-CU1 near its apical third (Fig. 83).
Legs. Hind coxa very finely coriaceous and with satin sheen; length of hind femur, tibia and basitarsus 4.6, 4.7 and 5.3 times their width, respectively; middle tarsus 1.2 times as long as middle tibia; middle femur subparallel-sided and slightly slimmer than fore femur; hind tibia moderately inflated (Fig. 87).
Metasoma. Ovipositor sheath 14.4 mm, 1.1 times longer than body, 1.6 times as long as metasoma and 5.9 times as long as hind tibia, apex of sheath black; apical 0.5 of hypopygium incised (Fig. 84). Colour. Black; mandible brown and basally slightly darkened; base and apex of fore and middle tibiae, most of fore and middle basitarsi and subbasal ring of hind tibia ivory or pale brown; tegulae, base and apex of fore and middle femora, remainder of fore and middle tarsi (but middle telotarsus dark brown), hind tibial spurs, second-fifth metasomal segments, apical half of hypopygium and lateral spots on sixth tergite brown; pterostigma, veins and clypeus ventrally dark brown; wing membrane subhyaline.
Male. Similar to female, but sculpture of mesoscutum coarser (Fig. 90), head less emarginate posteriorly and propodeum more or less reticulate; third antennal segment 1.3 times as long as second segment, fourth antennal segment 1.9-2.1 times as long as third segment and 1.1-1.2 times as long as second and third segments combined, fifth antennal segment 1.9-2.3 times as long as third segment (Fig. 93); mouthparts partly ivory; paramere greyish setose and its apex black (Fig. 94); hind tarsus mainly dark brown or blackish. Variation. Body length of female 12.1-13.1 mm, of male 10.1-11.5 mm; length of malar space 0.2-0.3 times as long as second antennal segment; propleuron 0.8-0.9 times as long as mesoscutum in front of tegulae; ovipositor sheath 10.5-14.4 mm, 0.9-1.1 times longer than body, 1.4-1.6 times as long as metasoma and 4.1-5.9 times as long as hind tibia; occipital carina of female paratype narrow lamelliform medio-dorsally, mandible rather yellowish brown, hypopygium and sixth tergite entirely brown and seventh tergite laterally so, fore and middle legs (except coxae and trochanters) mainly brown, tegulae dark brown, hind femur brownish black and subbasal ring of hind tibia brownish.
Distribution. China (Ningxia, Inner Mongolia). Biology. Unknown. Etymology. Named after the collector, Prof. Dr Mao-Ling Sheng, for his contribution of our knowledge of Chinese parasitoid Hymenoptera.