A new species of Zagrammosoma Ashmead (Hymenoptera, Eulophidae) from Qinghai Province, China

Abstract The new species Zagrammosoma dulanense Cao & Zhu, sp. n., from Qinghai Province, China, is described and illustrated. All type specimens were reared from the pupae of Micrurapteryx sophorivora Kuznetzov & Tristan (Lepidoptera: Gracillariidae), a leafmining moth attacking the plant Thermopsis lanceolata R. Br. (Fabaceae). A key to the three known Asian species of Zagrammosoma is provided. All specimens are deposited in the Insect Collection, the Institute of Zoology, Chinese Academy of Sciences, Beijing, China.


Introduction
The genus Zagrammosoma Ashmead is one of several small genera of the Eulophidae tribe Cirrospilini (Hymenoptera: Chalcidoidea). The members of this genus mainly attack leafminers in the orders Lepidoptera and Diptera (LaSalle 1989), occasionally Coleoptera (Peck 1951) and Hymenoptera (Ubaidillah et al. 2000). They are predominantly New World in distribution. Noyes (2013) listed 16 species in this genus, with 12 of them known from the Americas (Gordh 1978, LaSalle 1989, Noyes 2013. Of the Old World species, Z. crowei (Kerrich) was known from East Africa and Reunion (Noyes 2013), Z. talitzkii (Bouček) from Italy and Eastern Europe through to Russia, Kazakhstan and Turkmenistan (Noyes 2013, Radeghieri et al. 2002, and Z. latilineatum Ubaidillah from Australia and Indonesia (Ubaidillah et al. 2000). Noyes (2013) also included Zagrammosoma variegatum (Masi) in Zagrammosoma. Several authors discussed differences between Zagrammosoma and Cirrospilus, which are clearly closely related (Gates 2000, Gordh 1978, Hansson and LaSalle 1996, LaSalle 1989, Ubaidillah et al. 2000, Ubaidillah et al. 2003, Zhu et al. 2002. For the most part these authors have placed variegatum Masi in the genus Cirrospilus as C. variegatus (Masi), and this paper follows that classification. It should be noted that a species of Cirrospilus determined as C. nr variegatus was included in a molecular analysis of Eulophidae relationships (Gauthier et al. 2000), and it consistently clustered with Cirrospilus rather than Zagrammosoma. This is despite the fact that a morphological analysis of Cirrospilini relationships (Ubaidillah et al. 2003) found that a relationship between Zagrammosoma and C. variegatus and the closely related C. afer (Silvestri) was supported by at least one morphological character. Until further work provides a better understanding of these relationships, this paper follows the definition of Zagrammosoma as used or discussed by Schauff et al. (1997), Zhu et al. (2002) and Ubaidillah et al. (2003), which excludes C. variegatus.
During a recent field trip to Kunlun Mountains, Qinghai Province, many specimens of a parasitoid species were reared from the pupae of Micrurapteryx sophorivora (Lepidoptera: Gracillariidae), a leafminer attacking Thermopsis lanceolata R. Br. (Fabaceae). These specimens are described and illustrated here as a new species of the genus Zagrammosoma, after comparing them with descriptions (Kerrich 1969, LaSalle 1989, LaSalle 1992, Ubaidillah et al. 2000, Yefremova 1995a, or specimens deposited in Natural History Museum (NHM), London, UK and those in the Insect Collection, the Institute of Zoology, Chinese Academy of Sciences (IZCAS), Beijing, China.
A key to the known Asian species of Zagrammosoma based on females is also provided.

Material and methods
Host plants were collected in Qinghai Province, China in late July 2013 and moved to the lab in Beijing to rear specimens of the leafminer moths and parasitoid wasps. Specialists in the Institute of Botany, Chinese Academy of Sciences, identified the plant. All parasitoid specimens were collected and stored in 95% alcohol. Then specimens were mounted on cards for morphological studies and deposited in the Insect Collection, the IZCAS, Beijing, China.
Habitus and head pictures were recorded with a NIKON D7000 digital camera connected to a NIKON SMZ 1500 stereomicroscope. Pictures of appendages (forewings, antennae and legs) were taken by a CANON 550D digital camera connected to a LEICA DM-2500 microscope. All pictures above were stacked with Helicon Focus software.
Unless indicated otherwise, all examined specimens are deposited in the Insect Collection, the IZCAS. Diagnosis. Vertex vaulted and extending above level of compound eyes; funicle 2-segmented; pronotum elongate; notaulus curved and extending to anterior half of axilla; axilla strongly advanced, typically elongate, mostly anterior to scutellum; mesoscutum elongate, longer than scutellum; scutellum with 2 pairs setae, and 2 parallel submedian grooves which are often difficult to discern due to color pattern; forewing often with fuscate areas; propodeum without plicae, but with remnants of a median carina; color at least partly yellow, often with striking patterns, not metallic. Biology. The biology of Zagrammosoma has been poorly studied, but its taxonomic host range seems to be quite wide but within a narrow ecological niche. Species are ectoparasitoids, mostly of the larvae or pupae of leafminers from several insect orders, including Lepidoptera and Diptera (LaSalle 1989), occasionally Coleoptera (Peck 1951) and Hymenoptera (Ubaidillah et al. 2000), and in total 15 families in the above four orders (Noyes 2013).
The key provided here will differentiate Z. dulanense from other Asian species; it can be distinguished from any New World species with even vaguely similar body coloration by the following characters of the forewing: surface of forewing (Fig. 3e) completely hyaline and without dark markings except for a very small patch near stigma, stigmal vein (particularly at base) and parastigma bordering marginal vein with dark areas in contrast to light colored marginal and postmarginal veins.
Color. Body yellow with black stripes and spots (Fig. 1b-d).
Frons yellow with two sets of short black stripes laterally extending from below the flange of vertex to upper lateral eye margin (Fig. 2b). Occipital foramen with a black spot. Two pairs of dark stripes diverging from occipital foramen, one pair diverging upward to the anterior ocellus, truncated into two pieces by posterior ocelli, and the other pair proceeding ventrally and curving antero-dorsally to meet ventral eye margin (Fig. 2a). Antenna yellow, scape with a oblique black stripe on dorsal surface, pedicel with a black spot basally on dorsal surface (Fig. 3d).
Pronotal collar and lateral lobe of mesoscutum pale yellow. A black stripe extending from base of pronotum to apex of scutellum medially, forming a reverse triangle on dorsellum. Two enlarged dark spots anterolaterally on mesoscutum, which are partially visible through the pronotum which overlaps them. Mesoscutum with dark stripe bordering axilla. Two parallel black stripes on lateral lobe of mesoscutum in lateral view. Acropleuron and upper mesepimeron with a dark stripe respectively; sometimes the one on upper mesepimeron truncated into two short parts. The border of metapleuron covered by dark stripe. Dark stripes along notauli and scuto-scutellar suture. Two dorsolateral dark stripes on scutellum, slightly diverging anteriorly and fused posteriorly. Lateral panel of metanotum with short black curved stripe. Propodeum with a dark stripe along the anterior margin and a W-shaped dark marking below it; the median line of "W" bold basally and apically, reaching the anterior margin.
Metasoma yellow with black coloration pattern (Fig. 1b-d). Black markings on Gt 1 -Gt 5 extend postero-laterally and develop the forms of "W" with straight or arched stripes below them; sometimes these stripes absent. Markings on Gt 6 and Gt 7 reduced to three black spots respectively. Wings hyaline; vein pale yellow with the exception of fuscate parastigma and STV; SMV with a black line on it; humeral plate and tegula with one dorsal dark spot respectively. Legs (Fig. 3a-c) yellow; middle and hind coxae with dark dorsal spot; hind femur with black stripe on dorsal surface extending from base approximately three quarters the length of femur, and a black spot near apex of femur.
Head: Head ( Fig. 2a-b) nearly quadrate in anterior view, with numerous short white setae. Mandible brown apically. Vertex with several scattered black setae dorsally, vaulted between compound eyes. Face with small and scattered white setae, difficult to see due to the coloration pattern. Eyes bare. Toruli placed slightly above the level of lower eye margin. Relative measurements: POL 12, OOL 8.
Antenna: Antenna (Fig. 3d) with two anelli, two funicular segments and a 3-segmented club. The first funicle slightly longer than the second segment with ratio of length 11/9; the first funicle slightly longer than its width, the second segment as long as wide. Ratios of the length of three club segments: 8/6/6; the second club segment more transverse. All segments excluding scape and anelli setose with several fuscate setae in dorsal view. Longitudinal sensilla present on all funicular and club segments.
Mesosoma: Mesosoma ( Fig. 1b-d) with fine reticulate sculpture dorsally and laterally, and several short white setae scattered on the midlobe of mesoscutum. Notaulus curving to meet axilla. Scutellum with 2 pairs of long white setae. Lateral panel of metascutum smooth; dorsellum large, triangular, the tip pointed. Propodeum with fine reticulate sculpture, callus with some white erect setae, spiracle small and round.
Metasoma: Metasoma with fine reticulate sculpture, pointed apically. Short white setae uniformly distributed on metasoma. Metasoma subequal in length with mesosoma, and slightly wider. Length ratio of metasoma/mesosoma: 100/105; width ratio of metasoma/mesosoma: 60/55. Petiole very short and transverse, not visible in dorsal view. Three dark cercal setae present, which are slightly different in length. Tips of ovipositor sheath visible dorsally.
Legs. Legs (Figs 3a-c) with numerous setae on tibiae and tarsi. Tibial spur on each leg shorter than basitarsus, particularly on fore leg.
Forewing: Forewing (Fig. 3e) length 1.5-1.8 mm, with large bare areas extending from base of basal cell to STV except for several admarginal setae on ventral surface of wing below MV. Costal cell with several pale setae on its dorsal surface. SMV with 5-10 dorsal setae, MV with a row of black setae. SMV longer than MV; PMV shorter than STV. Relative lengths of veins: SMV/MV/PMV/STV: 60/40/10/19. Several black setae on STV, stigma long and slightly curved, with uncus near its apex. The triangular area on wing surface between PMV and STV bare. Speculum open. Basal setal line absent. Cubital setal line absent at base, and its three or less setae extend into speculum. Subcubital line very close to the margin of forewing.
Variation: Apart from different body sizes of specimens, the main variation is in the color pattern, particularly on propodeum and metasoma. On propodeum, the lateral arms of W-shaped markings may not connect to the posterior transverse marginal stripe. On metasoma, variations include changes in thickness of stripes and whether the black transverse stripes below the W-shaped dark markings exist, and if exist, whether connecting to the W-shaped dark markings. Occasionally, there is a small dark spot between the toruli.
Male: Smaller than female. Body length 1.8-2.3 mm. Forewing length 1.3-1.6 mm. Antenna with numerous setae on flagellar segments, more setose than that of female. The significant difference between female and male lies in the pattern of stripes on metasomal tergites, which are often paler and less extensive than that of female (Fig. 1a). Gt 7 shorter than other metasomal tergites by comparison, and markings on it reduced to one black spot. Genitalia protruding in dorsal view.
Biology: The new species has been reared from the pupae of Micrurapteryx sophorivora Kuznetzov & Tristan (Lepidoptera: Gracillariidae) on Thermopsis lanceolata R. Brown (Fabaceae). Gençer and Seven (2005)   The host plant is toxic and can cause livestock poisoning, but has also been used as a Chinese medicine plant (Zhu and Kirkbride 2006). Adults emerged from the host moth throughout August 2013, with fewer female specimens reared in September, while three males were collected in October. To our surprise, another female was captured from the dry host plant kept in the lab until mid May, 2014.
Etymology. This species is named for the locality in Dulan County, Qinghai Province, China, where the host plant, moth and type specimens were collected.

Key to the known Asian species of Zagrammosoma based on females
Note that some species of Cirrospilus, e.g. C. variegatus, appears very close to Zagrammosoma, and even have a slightly to distinctly vaulted vertex. These species of Cirrospilus can be distinguished by having the notaulus straight posteriorly and extending to the scuto-scutellar suture. Dr Yi-Bo Luo, Dr Jin-Zheng Zhang and Dr Qin-Wen Lin (Institute of Botany, Chinese Academy of Sciences) helped us in identification of the host plant. Dr Chun-Sheng Wu (IZCAS) identified the host leaf-miner. We also appreciate papers offered by Dr Zoya Yefremova (Ulyanovsk State Pedagogical University). We are grateful to the following lab members: Mr Liang Ding, who found the mined plants first during field collections in 2007 and 2013; Mr Qing-Tao Wu helped a lot for long-distance driving and transportation from Beijing; Dr. Ze-Qing Niu, Dr. Ying Wang, Xu Zhang and Feng Yuan for their comments on parts of this manuscript.
Finally, we appreciate comments and corrections from Dr. Gary Gibson, two anonymous reviewers and the Section Editor, Dr. Michael Engel. Their helps and comments greatly improved the quality of this manuscript for publication.