Anastatus (Anastatus) japonicus Ashmead, 1904

Peng, Lingfei, Gibson, Gary A. P., Tang, Lu & Xiang, Jiawei, 2020, Review of the species of Anastatus (Hymenoptera: Eupelmidae) known from China, with description of two new species with brachypterous females, Zootaxa 4767 (3), pp. 351-401 : 381-386

Anastatus (Anastatus) japonicus Ashmead, 1904

Figs 15–17

Anastatus japonicus Ashmead, 1904: 153 . Described: both sexes.

Anastatus japonicus ; Kalina, 1981: 17–19, plate 1, fig. 6; Yang et al., 2015b: 163–164, 255, fig. 84.

Anastatus (Anastatus) japonicus ; Narendran, 2009: 82, figs 26, 27.

Anastatus (Anastatus) japonicus ; Chen et al., 2019: 126–128 , fig. 5.

Anastatus bifasciatus disparis Ruschka, 1921: 265 . Synonymy by Bouček, 1977: 124–124.

Anastatus disparis ; Burgess, 1929: 574 (new status).

Anastatus flavipes Sheng and Wang, in Sheng et al., 1997: 6–7 (Chinese description). 8 (English abstract), figs 10–13. New synonymy.

Anastatus dendrolimus ; Xiao et al., 2001: 204. Misidentification.

Anastatus colemani ; Hu et al., 2011: 483, fig. 2. Misidentification.

Anastatus tenuipes ; Hu et al., 2011: 483–484. Misidentification.

Anastatus flavipes ; Peng et al., 2017: 7–10 , figs 8–18.

Diagnosis. Female. Macropterous ( Figs 16 A–C, E). Fore wing with hyaline cross band behind marginal vein com- plete and with entirely white setae ( Fig. 15F ); infuscate region basal of hyaline band with uniformly dark setae or sometimes with region of paler, more orangish setae anterior to cubital fold ( Figs 15F , 16F ), but about 2.0–2.5× as wide as cross band ( Fig. 15F ); basal region with basal cell, mediocubital fold and cubital and vanal areas setose, though at least basal cell with comparatively inconspicuous white setae ( Fig. 16F ). Head with scrobal depression separated from anterior ocellus by distance about equal to 1.2–2.0× longitudinal diameter of ocellus ( Figs 15 A–C: lines indicate approximate distances). Antenna ( Fig. 15D ) with fl2 longer than pedicel but not all funiculars longer than wide, with at least apical two funiculars quadrate to slightly transverse ( Fig. 15E ). Mesosoma with mesonotum ( Figs 16G, H ) dark, usually variably distinctly metallic green except concave posterior part of mesoscutum reddishviolaceous to partly blue or purple, but pronotum, procoxa, prepectus, and at least about posterior half of acropleuron contrastingly paler, reddish-brown to yellow ( Figs 16 C–E); mesotibial apical spur pale ( Figs 15G , 16A, C, E ); mesotarsus often with all tarsomeres pale in contrast with dark mesotarsal pegs but sometimes basal two tarsomeres and apical one or two tarsomeres variably distinctly infuscate ( Figs 15G , 16A, C, E ). Mesoscutum ( Figs 16G, H ) with convex anterior part of medial lobe entirely punctate-reticulate, and with posterior concave part of mesoscutum broadly setose with white setae; mesoscutal lateral lobe with bare, minutely mesh-like-coriaceous band anterior of posteromedian carina relative to more oblique, coriaceous-alutaceous sculpture on outer inclined surface ( Figs 16G, H ). Profemur with ventral margin evenly curved, without distinct angulation or tooth apically ( Fig. 1H ).

MALE. Antenna ( Figs 17E, F ) with scape entirely dark (examined syntype, Fig. 17F ) to variably extensively yellow ( Fig. 17E ); flagellum uniformly dark such that multiporous plate sensilla not contrasting in colour with surrounding cuticle, and consisting of clava and seven funiculars, the clava variably shorter than ( Fig. 17G ) to longer than (examined syntype, Fig. 17 H ) combined length of fl6–fl8. Head ( Fig. 17F ) with frons mesh-like coriaceous. Mesopleurosternum uniformly dark ( Figs 17 A–C). Legs beyond trochanters at least with all femora and metatibia mostly dark ( Figs 17 A–C), with mesotibia usually entirely pale ( Figs 17B, C ), but type males with about apical half of mesotibia dark ( Figs 17A, J ). Fore wing ( Fig. 17I ) with costal cell dorsally setose along entire leading margin; basal cell entirely, uniformly setose with dark setae; disc with variably large but often comparatively slender, oblique speculum ( Fig. 17I : spc) closed posteriorly by line of dark setae.

Species concept. Our concept of A. japonicus is based on examination of one female labelled “ Japan | Koebele / CoType | No. 7168 | U.S. N.M” and one male labelled “ Japan | Koebele / ♂ Type | No. 7168 | U.S. N.M”, plus online images of a second similarly labelled USNM female available at: www.usnmhymtypes.com/default. asp?Action=Show_Types&Single_Type=True&TypeID=3511). This latter female is labelled as “ ♀ type” and is segregated in the USNM type collection, but all the remaining type specimens of A. japonicus are syntypes because Ashmead (1904) did not originally designate a holotype.

Our concept of A. flavipes is based on examination of the female holotype, male allotype, and remaining 11 female and 5 male paratypes (FAFU) from Jiangxi and Shandong provinces, China as detailed by Peng et al. (2017).

Regional records. Anastatus japonicus was reported previously from China by several authors (see references in Noyes 2019), though at least some of the records associated with parasitism of T. papillosa from mainland China are misidentifications of A. fulloi (see under latter species). The species has not previously been reported from Taiwan, where we confirm it as a parasitoid of T. papillosa .

Regional material examined. Anhui: Bao’er-shan, Quanzhai, 16.VIII.1982, B. Luo (1♀ IZCAS). Beijing: Arboretum near Temple of Sleeping Buddha, 5.VII.1992, H.W. Browning, on Juglans regial [sic] (1♀ CNC). Ciyun Temple, 31.VII.1956, D. Zhang (1♀ IZCAS). Dashankou, 23.VII.1955, D. Zhang (1♀ IZCAS). Haidian, 7.VII.2013 (1♀ FAFU), 2013 (2♀, 1♂ FAFU), VII.2014 (1♀, 2♂ FAFU). Haidian, Baiwang Mountain, VIII2014, J. Zhang and T. Haye, ex. eggs Halyomorpha halys on Robina trees (21♀, 3♂ CNC), VII.2015, ex. eggs Cappaea tibialis on Robina trees (12♀, 4♂ CNC). Haidian, Baiyushan, VII.2015 (2♀, 1♂ FAFU). Haidian, Lengquan village, 2013, J. Zhang and T. Haye, ex. eggs Plautia fimbriata on mulberry tree (19♀, 18♂ CNC), VII.2014, ex. eggs Dolycoris baccarum (L.) (7♂ CNC), ex. eggs Menida violacea Motschulsky, 1861 (10♀, 3♂ CNC). Haidan, Miaofeng Mountain, VIII.2014, J. Zhang and T. Haye, ex. eggs Halyomorpha halys on Robinia trees (7♀ CNC). Haidian, Shengshuyuan, 2013, J. Zhang and T. Haye, ex. eggs Plautia crossota on mulberry trees (10♀, 13♂ CNC), 18.VI.2013, ex. eggs Halyomorpha halys on Robinia trees (3♀, 5♂ CNC). Xishan, VIII.2014 (2♀ FAFU). Fujian: V.1992, Lin, reared from Tessaratoma papillosa Drury (15♀, 12♂ CNC). Gansu: Kang Country, Longnan City, 23.I.2018, Y. Chen, ex. Caligula japonica Moore egg, laboratory reared on Antherea pernyi (Guérin-Méneville) eggs (24♀, 18♂ CNC). Hainan: Nankai, Baisha County, 14.V.2009, T. Hu, light trap, IOZ(E) 1812020 (1♀ IZCAS). Hebei: Langfang City, 26.VII.2013 (1♀ FAFU). Jiangxi: Bamian Mountain, Huangyangjie, Jinggang Mountains, 29.VII.2014, Q. Liu (1♀ FAFU). Jilin: campus of Jilin Agriculture University, Changchun City, 25.VI.2017, Y. Chen (1♀ FAFU). Campus of Jilin Agricultural University, Changchun City, 20.VII.2017, Y. Chen, ex. laboratory reared eggs of Antherea pernyi (36♀, 21♂ CNC). Liaoning: Tai Shan Shan Forest Farm, Manchu Autonomous County, Benxi City, 23.IV.2017, Y. Chen, ex. Caligula japonica egg, laboratory reared on Antherea pernyi (Guérin-Méneville) eggs (29♀, 18♂ CNC). Shaoguoyingzi, Jianping, 23.VIII.1982 (1♀ IZCAS). Shaanxi: Haoping, Taibai Mountains, Malaise trap, 26.IX.2014, Z. Yang (1♀ FAFU). Shanxi: Lingqiu, 9.VIII.1984, X. Gao (2♀ IZCAS). Taiwan: Miaoli, field collect- ed from T. papillosa eggs in 2015 and laboratory reared on T. papillosa eggs, Y.-H. Wu (15♀, 12♂ CNC), laboratory reared in National Chung Hsing University, 30.VII.2017 (1♀ FAFU). Taipei, 24.037267°N 120.687722°E, V.2018, J.-C. Hsu, laboratory reared (F2) 12.IX.2018, Tessaratoma papillosa (2♀ CNC). Taipei, field collected from T. papillosa eggs and laboratory reared on Samia cynthia eggs, 24.VT.2017, Y.-H. Wu (7♀, 4♂ CNC). National Taiwan University, Taipei, 28.X.2015, Y.-H. Wu, from Tessaratoma papillosa (7♀, 1♂ CNC). Taipei Botanical Garden, Taipei, VIII.2016, L.-J. Wang (1♀ CNC). Zhejiang: Tianmu Mountains, 5.VII.2014 (4♀ FAFU), 27.IV.2014 (1♀, 1♂ FAFU), reared from egg of Hippotiscus dorsalis, H.E. Sunqiang.

Distribution. Regional. ORIENTAL: China (Fujian, Guangdong, Guangxi, * Hainan, Hong Kong, Jiangsu, *Jiangxi, * Taiwan, *Zhejiang). PALAEARCTIC: China: (* Anhui, Beijing, * Gansu, * Hebei, * Heilongjiang, Jilin, Liaoning, Shaanxi, Shanxi, Shandong).

Extralimital. Noyes (2019) reported A. japonicus from at least one country from all biogeographic regions except the Neotropics. It is widely distributed throughout the entire Palaearctic Region where it is native, but presence in Canada and United States of America (Nearctic) results from secondary introductions associated with biocontrol of Lymantria dispar (Linnaeus, 1758) ( Lepidoptera : Erebidae ) ( Crossman 1925).

Hosts. Noyes (2019) reported A. japonicus as a parasitoid of over 15 host species in two families of He- miptera ( Alydidae , Pentatomidae ) and five families of Lepidoptera ( Lasiocampidae , Lymantriidae , Notodontidae , Papilionidae , Saturniidae ), sometimes as a hyperparasitoid through Braconidae ( Hymenoptera : Ichneumonoidea) and Encyrtidae ( Hymenoptera : Chalcidoidea) primary parasitoids. Hu et al. (2011), under the misidentification A. colemani , reported Rhynchocoris humeralis as a host, and Chen et al. (2019) newly reported Caligula japonica as a host. New host records reported here are Cappaea tibialis Hsiao and Cheng, 1977 , Dolycoris baccarum (Linnaeus, 1758) , Halyomorpha halys (Stål, 1855) , Menida violacea Motschulsky, 1861 and Plautia crossota (Dallas, 1851) ( Hemiptera : Pentatomidae ). These last records, from specimens originally collected by J. Zhang and T. Haye, represent voucher material from Zhang et al. (2017), in which the parasitoid was identified as Anastatus species. Noyes (2017) also recorded seven plant families as associates of A. japonicus . Here we newly report Juglans regia L. ( Juglandaceae ), and the genera Morus L. ( Moraceae ), and Robinia L. ( Fabaceae ).

As is also discussed under A. formosanus and A. fulloi , A. japonicus apparently is an important parasitoid of T. papillosa in Taiwan, but in southern China it is replaced by A. fulloi as the principal biocontrol agent. Because A. fulloi appears to have been consistently misidentified as A. japonicus in mainland China, the extensive biological literature published under this name in China is brought into question. Li et al. (2014) listed four “challenges” for the implementation of integrated pest management in litchi orchards in China. To this list should also be added a fifth challenge, accurate taxonomy of the biocontrol agents.

Remarks. Females we interpret as A. japonicus are distinguished by a combination of features, being most similar to those of A. fulloi and A. orientalis because of a partly pale mesosoma and absence of a profemoral tooth. However, females we identify as A. fulloi and A. orientalis have a uniformly dark acropleuron with slight metallic luster ( Figs 10F , 20F ) similar in colour to the mesonotum ( Figs 10E , 20E ) whereas females we identify as A. japonicus have the acropleuron variably extensively but noticeably paler than the mesonotum, at least non-metallic brown posteriorly ( Fig. 16C ), and usually conspicuously paler orangish to yellow over at least about its posterior half ( Figs 16D,E ). Females also have the scrobal depression distinctly separated from the anterior ocellus ( Figs 15A, C ), though this distance varies among females we examined. The exact distance between the anterior ocellus and dorsal margin of the scrobal depression can be difficult to measure accurately because the dorsal margin of the depression often is only indistinctly developed. However, the examined female A. japonicus syntype has the scrobal depression separated from the anterior ocellus ( Fig. 15A : osd) by almost twice the longitudinal diameter of the ocellus. Females from western Europe and type females of A. flavipes ( Fig. 15B ) have the scrobal depression separated from the anterior ocellus by about 1.5–2.0× an ocellar diameter, but many eastern Palaearctic females have the scrobal depres- sion separated by as little as 1.2× an ocellar diameter, more similar to that of females of A. fulloi ( Fig. 10C ) and A. orientalis ( Fig. 20C ). There is also variation in mesotarsal colour pattern that appears to form a continuum among females of A. japonicus , A. fulloi , and A. orientalis . Females of A. orientalis have entirely pale mesotarsi ( Fig. 20H ) whereas A. fulloi females often have entirely infuscate mesotarsi, but at least the dorsal and posterior surfaces of the basal two tarsomeres are noticeably darker than the following two tarsomeres ( Fig. 10H ). However, some females we identify as A. japonicus have entirely pale mesotarsi ( Fig. 16D ) similar to A. orientalis females, whereas others have the basal two tarsomeres and sometimes the apical one or two tarsomeres infuscate similar to some A. fulloi , including the syntype of A. japonicus we examined ( Fig. 15G ) and the USNM-imaged syntype. If there are associated males, it is easy to distinguish A. orientalis because males of this species have entirely yellowish legs ( Fig. 21B ) or at most the metafemur variably dark ventrally ( Fig. 21E ) as well as basally pale antennae ( Fig. 21G ). However, we cannot presently distinguish males of A. japonicus from those of A. fulloi reliably, and because of observed variation among females of the two species confident identification of the species sometimes is difficult. Even our present concept of A. japonicus requires further study. Ashmead (1904: 153) originally described males as having the legs “aeneous-black…an annulus at base of the tibiae…white”, and when Crawford (1913: 249) described A. formosanus he stated that the species resembled A. japonicus but in males of the latter species “the middle tibiae are dark”. The male syntype of A. japonicus we examined ( Fig. 17A ) has about the apical half of the mesotibia dark ( Fig. 17J ). There are three other male syntypes of A. japonicus in the USNM, only one of which has the mesotibiae remaining, but this also has the mesotibiae darkened apically, whereas other USNM males from China, Iran, Japan, Spain, and the United States of America have entirely pale mesotibiae (Michael Gates, personal communication) as do all the males we record from China as well as males identified as A. japonicus from Canada and the United States of America in the CNC. Further, the examined male syntype has the clava quite distinctly shorter than the combined length of the apical three funiculars ( Fig. 17H ), whereas other males we identify as A. japonicus have the clava at least as long as the apical three funiculars ( Fig. 17G ). Apparent variation in relative length of the clava was also noted for A. fulloi (see further under this species) and it remains questionable whether this indicates intraspecific variation in the species or possibly unrecognised cryptic species. However, the presence of apically dark mesotibiae for type series males but entirely pale mesotibiae for all subsequently identified A. japonicus males, even those from Japan (e.g., Tachikawa (1959) under the name A. bifasciatus ), is certainly anomalous. Ashmead (1904: 153) stated that A. japonicus was described “from several specimens received from Mr. A. Koebele”. The implication is that the association of the sexes was based on their being reared together, though there is no explicit statement of this in the publication or labelling. Three possibilities could explain the apparent anomalous leg colour pattern—1) males of A. japonicus are conspicuously variable in mesotibial colour pattern, which seems unlikely based on the diversity of subsequently reared specimens examined; 2) the type material of A. japonicus was not reared and is a mixed series with females and males belonging to different species; or 3) A. japonicus has been incorrectly interpreted subse- quent to the original description and all literature records, including our own, actually represent some other very similar but much more widely distributed species. If the latter, the correct name would be the current oldest junior synonym Anastatus disparis because Ruschka (1921: 266) described the male as having the “legs brown, femora green, front and middle tibiae and the tarsi except the last segment yellow”. We also newly synonymise A. flavipes under A. japonicus . Females of the type series of A. flavipes are somewhat unusual in having the acropleuron entirely pale ( Peng et al. 2017, fig. 9) or almost so ( Fig. 16D ), but otherwise are typical of females we recognise as A. japonicus , including having the scrobal depression and anterior ocellus comparatively widely separated ( Fig. 15B ), as noted above. Type males of A. flavipes are similar in leg colour pattern and antennal structure ( Peng et al. 2017, figs 15–18) to other non-type males we recognise as A. japonicus . Because of the unusually wide world distribution of A. japonicus , even if sometimes the result of intentional introductions, as well as diverse host records and morphological diversity of both sexes, molecular analyses are required to investigate whether our current concept of A. japonicus includes one or more cryptic species.

Figures

FIGURE 1. Anastatus (Anastatus) bifasciatus female. A, Dorsal habitus (2018-72); B, lateral habitus (2018-72); C, antenna (2018-72) [insert: pedicel and basal two flagellomeres]; D, fore wing (2018-73); E, frontal head (2018-72); F, base of fore wing (2018-73); G, mesonotum (2018-72); H, profemur, posterior view (2018-82); I, mesotibial apical spur and mesotarsus (2018-82).Abbreviations: aod = longitudinal diameter of anterior ocellus, bac = basal cell, cua = cubital area, flx = flagellomere number, mcf = mediocubital fold, mdf = medial fold, osd = distance between anterior ocellus and scrobal depression, pdl = pedicel, vna = vanal area.

FIGURE 10. Anastatus (Anastatus) fulloi female. A, Dorsal habitus (2019-13) [insert: propodeum]; B, lateral habitus (2019- 12) [insert: mandibles]; C, head frontal (2019-15); D, antenna (2019-14) [insert: apical two funiculars and clava, vertical lines indicate length of antennomeres]; E, dorsal mesosoma (2019-13); F, lateral mesosoma (2019-12); G, fore wing (2019-14); H, mesotibial apical spur and mesotarsus (2019-12). Abbreviations: aod = longitudinal diameter of anterior ocellus, osd = distance between anterior ocellus and scrobal depression.

FIGURE 15. Anastatus (Anastatus) japonicus female. A, frontal head (A. japonicus syntype); B, frontal head (A. flavipes paratype); C, frontal head (2019-43); D, antenna (A. japonicus syntype); E, apical four funiculars and clava (2019-43); F, fore wing (2019-46); G, mesotibial apical spur and mesotarsus (A. japonicus syntype). Abbreviations: aod = longitudinal diameter of anterior ocellus, clv = clava, flx = flagellomere number, osd = distance between anterior ocellus and scrobal depression, pdl = pedicel.

FIGURE 16. Anastatus (Anastatus) japonicus female. A, Dorsal habitus (A. japonicus syntype); B, dorsal habitus (2019-6); C, lateral habitus (A. japonicus syntype); D, lateral habitus (A. flavipes paratype); E, lateral habitus (2019-4); F, base of fore wing (2019-6); G, dorsal mesosoma (A. japonicus syntype); H, dorsal mesosoma (2019-6).

FIGURE 17. Anastatus (Anastatus) japonicus male. A, Lateral habitus (A. japonicus syntype); B, lateral habitus (A. flavipes paratype); C, lateral habitus (2019-25); D, dorsal head and mesosoma (A. japonicus syntype); E, antenna (2019-25); F, head and antenna (A. japonicus syntype). G, apical three funiculars and clava (2019-25); H, apical three funiculars and clava (A. japonicus syntype). I, fore wing (A. japonicus syntype); J. mesotibia and tarsus (A. japonicus syntype). Abbreviations: clv = clava, flx = flagellomere number, spc = speculum.

FIGURE 20. Anastatus (Anastatus) orientalis female. A, Dorsal habitus (2019-48); B, lateral habitus (2019-47); C, head frontal (2019-49); D, antenna (2019-48) [insert: apical three funiculars and clava, vertical lines indicate length of antennomeres]; E, dorsal mesosoma (2019-48); F, lateral mesosoma (2019-47); G, fore wing (2019-47); H, mesotibial apical spur and mesotarsus (2019-47). Abbreviations: aod = longitudinal diameter of anterior ocellus, osd = distance between anterior ocellus and scrobal depression.

FIGURE 21. Anastatus (Anastatus) orientalis male. A, Dorsal head and mesosoma (2019-52); B, lateral habitus (2019-50); C, frontal head (2019-51); D, frontovertex (2019-51); E, lateral mesosoma (2019-53) [arrows point to pale bands on mesepisternum]; F, fore wing (2019-52); G, antenna (2019-51); H, base of fore wing (2019-52). Abbreviations: fml = femoral line, spc = speculum, tsl = transepisternal line.