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Academic editor: Andreas Köhler
© 2019 Yong-Ming Chen, Gary A. P. Gibson, Ling-Fei Peng, Asim Iqbal, Lian-Sheng Zang.
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Citation:
Chen Y-M, Gibson GAP, Peng L-F, Iqbal A, Zang L-S (2019) Anastatus Motschulsky (Hymenoptera, Eupelmidae): egg parasitoids of Caligula japonica Moore (Lepidoptera, Saturniidae) in China. ZooKeys 881: 109-134. https://doi.org/10.3897/zookeys.881.34646
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Four species of Anastatus Motschulsky (Hymenoptera, Eupelmidae, Eupelminae) are newly reported as egg parasitoids of the Japanese giant silkworm, Caligula japonica Moore and, as an alternate laboratory host, the Chinese oak silk moth, Antheraea pernyi (Guérin-Méneville) (Lepidoptera, Saturniidae) in China. The four species, A. fulloi Sheng & Wang, 1997, A. gansuensis Chen & Zang, sp. nov., A. japonicus Ashmead, 1904, and A. meilingensis Sheng, 1998, were reared initially from eggs of C. japonica collected in Gansu, Jilin and Liaoning provinces and subsequently cultured in the laboratory on eggs of A. pernyi. An illustrated key to differentiate females of the four species, and males of some of the species is provided. Key features are illustrated, both sexes of the new species are described, and diagnoses of females of the other species are given.
Antheraea pernyi, Chalcidoidea, natural enemy, new species, parasitic wasp, taxonomy
The Japanese giant silkworm, Caligula japonica Moore, 1862 (Lepidoptera, Saturniidae), is a widely distributed indigenous species in China, being reported previously from both Palaearctic (Heilongjiang, Jilin, Liaoning, Hebei, Shandong, Shaanxi) and Oriental (Chongqing, Fujian, Gansu, Guangdong, Guangxi, Guizhou, Hubei, Hunan, Jiangxi, Sichuan, Taiwan, Yunnan, Zhejiang) provinces (
Prior to the present study, seven species of Chalcidoidea (Hymenoptera) have been reported as parasitoids of C. japonica (sometimes cited under the combination Dictyoploca japonica), including a single species of Chalcididae (Kriechbaumerella hofferi (Bouček, 1952)), another of Encyrtidae (Ooencyrtus dictyoplocae Sharkov, 1995) and Eulophidae (Aprostocetus brevipedicellus Yang & Cao, 2015), two species of Eupelmidae (Mesocomys albitarsis (Ashmead, 1904) and M. kalinai Ozidikmen, 2011) and of Trichogrammatidae (Trichogramma chilonis Ishii, 1941 and T. dendrolimi Matsumura, 1926) (
Species of Anastatus Motschulsky (Eupelmidae, Eupelminae) are mostly primary parasitoids of the eggs of other insects, although a few have been reared as secondary parasitoids (hyperparasitoids) of Lepidoptera eggs through Scelioninae (Platygastroidea, Platygastridae) and Ichneumonidae (Ichneumonoidea) primary parasitoids, and some have been reared from Coleoptera larvae and Diptera puparia (
Several species of Anastatus have been used for biological control of various insect pests in China and elsewhere (
Surveys and rearing of specimens on which this study is based were conducted by Yong-Ming Chen, Lian-Sheng Zang and Asim Iqbal. Surveys were conducted in three provinces in China that were infested with C. japonica, one province in north-central China (Gansu, Kangxian County, 33°26'33.81"N, 105°41'52.10"E in January to March, 2017 and 2018) and two provinces in north-eastern China (Jilin, Changchun City, 43°48'29.09"N, 125°24'14.03"E in July to August, 2017, and Liaoning, Benxi County, 41°14'56.40"N, 124°28'55.06"E in March, 2017). The overwintering egg masses collected in the field surveys were placed into glass tubes and the opening of each tube covered with a small piece of cloth. The glass tubes were kept in a rearing chamber kept 25±1° C and 70±5% RH, with a 14 L: 10 D photoperiod until the wasps emerged. The sex ratio = was calculated as the number of females/(number of females + number of males). Emerging wasps were then used to establish colonies at Jilin Agricultural University using fresh and healthy unfertilized eggs of A. pernyi that were obtained by dissecting female abdomens as per
Random samples of reared colony individuals were preserved in 75% ethanol for further use, with specimens used for morphological study and collection deposition either air dried and point-mounted at JLAU or critical-point dried from ethanol and point-mounted at
Morphological and sculptural terms follow
AICF Al. I. Cuza University, Iaşi, Romania, Lucian Fusu collection;
FAFU Biological Control Research Institute, Fujian Agriculture and Forestry University, Fuzhou, China;
JLAU Institute of Biological Control, Jilin Agriculture University, Changchun, China;
From the cultures established from the surveys in Gansu Province, seven species were ultimately identified as egg parasitoids of C. japonica, belonging to two families and three genera (Anastatus (4 spp.) and Mesocomys (2 spp.) and Aprostocetus (1 sp.)). In 2017, three species were reared, A. gansuensis sp. nov., M. albitarsis (Ashmead) and M. trabalae Yao, Yang & Zhao, 2009. In 2018, all seven species were reared and identified as A. fulloi, A. gansuensis, A. japonicus, A. meilingensis, M. albitarsis, M. trabalae, and Aprostocetus brevipedicellus. The proportion of females to males under natural field conditions was 0.75, 1.00, 0.89, 0.75, 0.66, 0.66, and 0.77, respectively, for the seven species. In 2017 in Jilin Province only A. japonicus was reared, whereas in Liaoning province A. fulloi and M. albitarsis were reared. Their sex ratios were 0.82, 0.73, and 0.68, respectively. All seven species were reared successfully on the eggs of the alternative host, Antheraea pernyi, under laboratory conditions.
Anastatus Motschulsky, 1859: 116. Type species: Anastatus mantoidae Motschulsky, by monotypy.
Anastatus (Anastatus);
For a complete listing of the extensive generic synonymy of Anastatus see
1 | Female | 1 |
– | Male | 5 |
2(1) | Brachypterous, fore wings extending only to about posterior margin of Gt1 (Fig. |
A. meilingensis Sheng |
– | Macropterous, fore wings extending to apex of gaster (Figs |
3 |
3(2) | Acropleuron often dark anteriorly to about level of base of fore wing but variably paler, light brown to orangish or yellowish over at least posterior half (Fig. |
A. japonicus Ashmead |
– | Acropleuron entirely dark and not contrasting in color with mesonotum or at most somewhat paler anteriorly only near prepectus, the paler region not nearly extending to level of base of fore wing (Figs |
4 |
4(3) | Procoxa pale, orangish to yellowish (Fig. |
A. gansuensis Chen & Zang, sp. nov. |
– | Procoxa dark, much darker than lateral surface of pronotum and similar in color to prosternum (Fig. |
A. fulloi Sheng & Wang |
5(1) | Clava at least as long as combined length of previous three funiculars (Figs |
A. fulloi Sheng & Wang and A. japonicus Ashmead |
– | Clava shorter than combined length of previous three funiculars (Figs |
6 |
6(5) | Metatibia mostly similarly dark as femur, pale basally for distance only about equal to own apical width or about one-quarter or less length of tibia (Fig. |
A. gansuensis Chen & Zang, sp. nov. |
– | Metatibia with about basal half pale and apical half darker, though lighter brown than femur (Fig. |
A. meilingensis Sheng |
Anastatus fulloi Sheng & Wang in Sheng et al., 1997: 61–62, figs 14, 15; holotype (JLAU), examined.
Anastatus fulloi;
Female. Macropterous (Fig.
Anastatus fulloi A–E female: A dorsal habitus (13) B lateral habitus (12) C dorsal mesosoma (13) D lateral mesosoma (12) E fore wing (14). F–H male: F lateral habitus (22) G antenna (32) H clava and apical three funiculars (32) (three lower bars indicate length of clava compared to combined length of apical funiculars). Abbreviations: clv = clava, flx = flagellomere number.
Male. Structure plus color, setal and sculptural patterns (Fig.
Anastatus fulloi (Genbank accession no. MK604241) was described originally from Jiangxi Province from two localities (Wuyi Mountains and Meiling) (
The type series was reared from the eggs of the yellow spotted stink bug, Erthesina fullo (Thunberg, 1783) (Hemiptera, Pentatomidae). Here we newly report it as an egg parasitoid of the lepidopteran hosts C. japonica and, in the laboratory, A. pernyi.
Of the species we reared from C. japonica, females of A. fulloi are most similar to those of A. gansuensis because they are fully winged (cf. A. meilingensis) and have a dark acropleuron that does not contrast with the mesonotum (cf. A. japonicus). However, females differ from those of A. fulloi in color, setal and structural features, as given in the key to species and diagnoses.
Holotype ♀ (FAFU), Shanchacun, Yuntai Town, Kangxian County, Gansu Province, China, 01.III.2017, Yong-Ming Chen. Allotype ♂ (FAFU), same data as holotype (from subsequently established colony on A. pernyi).
Same data as holotype (2♀, 1♂ FAFU). Gansu Province, Kang Co., Longnan City, collected 23.I.2018, Yong-Ming Chen, ex. Caligula japonica Moore egg, lab reared on eggs of Antheraea pernyi (Guérin-Méneville) (Lep: Saturniidae) (2♀, 1♂ AICF; 2♀, 1♂
Female. Macropterous (Fig.
Anastatus gansuensis, female A dorsal habitus (9) B lateral habitus (7) C head in frontal view (10) D, same in dorsal view (9) E mesosoma in dorsal view (9) F same in lateral view (7) G antenna (10) H pedicel and basal three funiculars (10) I clava and apical three funiculars (10). Abbreviations: clv = clava, flx = flagellomere number; pdl = pedicel
Anastatus spp., female A–E A. gansuensis: A fore wing (8) B basal half of fore wing (29) C enlargement of medial part of wing disc (8) D gaster in dorsal view (9) E mesotarsus and apex of mesotibia, in anterior view (7). F, G A. fulloi, mesotarsus and apex of mesotibia (12): F in anterior view G in posterodorsal view. Abbreviations: Gtx = gastral tergite number, syn = syntergum.
Male. Legs with all femora mostly to entirely dark, mesotibia entirely pale, and metatibia mostly dark, pale basally for a distance at most equal to about apical width or about one-quarter length of tibia (Fig.
Anastatus gansuensis, male A dorsal habitus (17) B lateral habitus (16) C head in frontal view (19) D mesosoma in lateral view (16) E propodeum (17) F fore wing (17) G antenna (18) H pedicel and basal three funiculars (18) (three lower bars indicate length of clava compared to combined length of apical funiculars). Abbreviations: clv = clava, flx = flagellomere number.
Female (habitus, Fig.
Color.
Head (Fig.
Pronotum mostly pale (Fig.
Gaster (Fig.
Setation.
Head with slightly lanceolate, whitish-translucent setae on lower face, interantennal prominence, lower parascrobal region (Fig.
Pronotum mostly bare but with a few long, bristle-like setae in transverse line anterior to spiracle and similar seta medially on either side of mediolongitudinal groove (Fig.
Structure.
Head in frontal view (Fig.
Mesoscutum (Fig.
Gaster with ovipositor sheaths at least slightly protruding beyond syntergal flange (Fig.
Sculpture. Head with vertex and interocellar triangle transversely alutaceous to alutaceous-strigose, upper parascrobal region and frons to posterior ocelli on either side of anterior ocellus more mesh-like coriaceous to coriaceous-imbricate or coriaceous-granular, and lower half of parascrobal region reticulate-rugulose; lower face reticulate to reticulate-rugose; interantennal prominence reticulate-imbricate; scrobal depression mostly reticulate-imbricate.
Mesoscutum with convex anterior part of medial lobe uniformly punctate-reticulate, posteromedial concave part or medial lobe smooth and shiny, and lateral lobes mostly finely mesh-like coriaceous to alutaceous, with sculpture of inner inclined surfaces more distinct lateral of anteromedial lobe and much finer to smooth and shiny posteriorly near scutellar-axillar complex. Scutellar-axillar complex uniformly, similarly punctate-reticulate as convex part of medial lobe. Mesopleurosternum with anterolateral region finely mesh-like coriaceous but dorsally bare part near tegula more alutaceous-coriaceous; acropleuron mostly longitudinally strigose, more minutely centrally, sculpture dorsally and ventrally more longitudinally strigose-coriaceous and posteriorly mesh-like coriaceous with larger cell size.
Gaster (Fig.
Male (habitus, Fig.
Color.
Head with frontal surface (Fig.
Mesosoma (Fig.
Gaster mostly dark brown but with variably distinct metallic green luster dorsobasally on Gt1 (Fig.
Setation.
Head with very slightly lanceolate white setae on lower face, interantennal prominence and parascrobal region ventrally, but more hair-like dark setae on parascrobal region dorsally and frontovertex (Fig.
Structure.
Head in frontal view (Fig.
Structure of mesosoma and gaster (Fig.
Sculpture. Head with vertex reticulate-rugose to transversely reticulate-strigose; frons and parascrobal regions mesh-like coriaceous to granular, lower face shallowly reticulate to reticulate-imbricate.
Mesoscutum (Fig.
Anastatus gansuensis (Genbank accession no. MK373759) originally described from China (Gansu Province).
Solitary endo-parasitoid of the eggs of C. japonica in the field and, at least in the laboratory, of A. pernyi. Caligula japonica has one generation a year and overwinters in the egg stage; its egg-laying period is from late August to late October in northwestern China (
Derived from the name of the province in China from which the type series was originally collected through rearing.
Because of their dark acropleuron, females of A. gansuensis key most closely to females of A. fulloi in
Two features of the fore wing of female A. gansuensis are not apparent in all females: the presence of isolated dark setae within the hyaline cross band medially (Fig.
As noted under A. fulloi, a flagellar structure differentiates males of both A. gansuensis and A. meilingensis from those of A. fulloi and A. japonicus. Males of the former two species have the clava distinctly shorter than the combined length of the three apical funiculars (Figs
Anastatus japonicus
Ashmead, 1904: 153; syntypes (
Anastatus bifasciatus disparis
Ruschka, 1921: 265. Synonymy by
Anastatus disparis;
Anastatus japonicus;
Female. Macropterous (Fig.
Anastatus japonicus A–E female: A dorsal habitus (6) B lateral habitus (4) C mesosoma in dorsal view (6) D same in lateral view (4) E fore wing (5). F–H male: F lateral habitus (25) G antenna (25) H clava and apical three funiculars (25) (three lower bars indicate length of clava compared to combined length of apical funiculars). Abbreviations: clv = clava, flx = flagellomere number.
Male. Structure as well as color, setae and sculptural patterns (Fig.
Anastatus japonicus (Genbank accession no. MK604240) was reported previously from China (Beijing, Fujian, Guangdong, Guangxi, Hong Kong, Jiangsu, Jilin, Liaoning, Shaanxi, Shandong) by several authors (
Extralimital distribution listed for A. japonicus by
Females of A. japonicus are most easily distinguished from two species with macropterous females reared from C. japonica by the acropleuron being extensively paler, lighter brown to yellowish (Fig.
As noted under A. fulloi, males of A. japonicus and A. fulloi are differentiated from those of A. gansuensis and A. meilingensis by a longer clava relative to the combined length of the apical funiculars. This is because in A. fulloi (Fig.
Anastatus meilingensis Sheng, 1998: 5–6, fig. 1; holotype (JLAU), examined.
Anastaus meilingensis;
Female. Brachypterous, fore wing extending only to about level of posterior margin of Gt1 when body uncontorted (Fig.
Anastatus meilingensis A–E female (2): A dorsal habitus B lateral habitus C dorsal mesosoma D lateral mesosoma E fore wing, dorsal view. F–H male (19): F lateral habitus G antenna H clava and apical three funiculars (three lower bars indicate length of clava compared to combined length of apical funiculars). Abbreviations: cbr = remnant of hyaline cross band, clv = clava, flx = flagellomere number.
Male. Structure as well as color, setae and sculptural patterns (Fig.
Anastatus meilingensis (Genbank accession no. MK604242) was described originally from Jiangxi Province from three localities (Shangrao, Yushan, and Meiling, Nanchang) as detailed by
Originally described reared from the eggs of the pine moth, Dendrolimus punctatus Walker, and of the Simao pine moth, D. kikuchii Matsumura (Lepidoptera, Lasiocampidae) (Sheng and Yu 1988). Here we newly report it as an egg parasitoid of C. japonica and, in the laboratory, of A. pernyi.
Of the species we reared from C. japonica, females of A. meilingensis are readily distinguished because they are the only ones that are brachypterous. The fore wing color pattern, with the discal region having a distinct region of orangish setae behind the venation and often also a slender remnant of a hyaline cross band more apically (Fig.
Although
Our study newly demonstrates that Anastatus fulloi, A. gansuensis, A. meilingensis and A. japonicus are natural egg parasitoids of Caligula japonica and thus are potential biological control agents of this pest in China. Further, all four species were reared successfully on the eggs of the alternate host, A. pernyi in the laboratory, as for some Trichogramma species (
All Anastatus species previously reported have been considered to have a haplo-diploid reproductive mechanism, which requires fertilization of the female by a male for female production (
This research was funded by the National Key R&D Program of China (2017YFD0201000), National Natural Science Foundation of China (31301910), and Gansu Provincial Fiscal Science and Technology Award and Compensation Project (2018-01).