Andricus mairei ( Kieffer, 1906 ), 2001

Pujade-Villar, Juli, Wang, Yiping, Guo, Rui, Cuesta-Porta, Victor, Arnedo, Miquel A. & Melika, George, 2020, Current status of Andricus mairei (Kieffer), with synonymization of two species from China (Hymenoptera: Cynipidae), Zootaxa 4808 (3), pp. 507-525 : 510-517

Andricus mairei ( Kieffer, 1906)

Parandricus mairei Kieffer, 1906: 103 .

Andricus mairei (Kieffer) Melika & Abrahamson, 2001: 160 .

Andricus deqingis Wang, Gui, Chen, 2013: 976 n. syn.

Andricus flavus Pujade-Villar, Wang, Guo & Chen, 2014: 418 n. syn.

Diagnosis. Andricus mairei differs from other known Eastern Palaearctic sexual Andricus species by the following diagnostic characters: the malar area without carina irradiating from clypeus to eye margin and lower face; F 1 in male antenna straight, not curved, the pronotum is strongly rugose; the mesoscutum sculptured only anteriorly, along notaulus; tarsal claws are simple in males, and with a basal lobe in females; tarsal segments are very short in males; the prominent part of the ventral spine of the hypopygium relatively long, around 4.5 times as long as broad.

Type material of Andricus mairei : 1♂ collected by René Maire from Guizhou province in catkins of Quercus sp., presumably lost (supposedly deposited in ZAFU).

Studied material. Type material of A. deqingis (see comments, below): HOLOTYPE ♀ deposited in ZAFU, China: Zhejiang, Deqing , 1995.V.27, He Jun-hua, No. 965054 ; PARATYPES same data as holotype except for number (16 ♂ & 13♀) : 954460 (♀), 954461 (♂), 954462 (♀), 954463 (♀), 954468 (♂), 954471 (♀), 954472 (♀), 954473 (♀), 954475 (♂), 954476 (♂), 954478 (♂), 954713 (♀), 957885 (♀), 957888 (♀), 957913 (♂), 964480 (♀), 965051 (♂ UB) , 965052 (♂), 965053 (♀), 965055 (♂), 965056 (♂), 965059 (♀), 965060 (♂), 965061 (♂, UB) , 965062 (♂), 965067 (♂), 965068 (♂), 965069 (♂, UB) & 965115 (♀).

Type material of A. flavus (see comments, below): HOLOTYPE ♀, deposited in ZAFU, China, Zhejiang, Tianmushan (119°27′E, 30°19′N), (1.v.2011) 18.v.2011, Rui Guo, collected from gall reared in lab . PARATYPE 1♀, deposited in UB with same label as holotype.

Additional material examined. Same data as holotype of A. deqingis (not included in the typical series: 954482 (♀, UB), 959043 (♀), 959319 (♂), 959325 (♂, UB), 965057 (♀), 965058 (♀), 965070 (♂), 969297 (♂, UB), 978345 (♂), 978346 (♂) & 978347 (♂). Same data as holotype of A. flavus (not included in the typical series) 3♂ & 3♀ (1♂ & 2♀ UB); same data, (15.v.2011) 25.v.2011: 3♂ & 2♀; same data, (24.iv.2011) 25.iv.2011: 1♂; same data, (24. iv.2011) iv.2011: 1♀; same data, (24.iv.2011) 27.iv.2011: 8♂; same data, 119°45′E, 30°31′N, (21.v.2015) 7.vi.2015: 1♂ & 3♀ (1♀ UB), nº 6194 (S. Jie leg.). Mogan Muntain, Zhejiang, 27.v.1995: 1♂ (He Junhua leg.). Fengshuling, Changhua Town (Lin’an District, Hangzhou City, Zhejiang province), Q. glandulifera var. brevipetiolata Nakai , Dryocosmus sp 9 (leg. Guo Rui), (v.2014) 21.vii.2014: 15♂ & 4♀ (3♂ & 2♀ UB); same data, 28.vii.2014: 1♀ ( UB); same; same data, Andricus sp5, (28.iv.2014) 16–v.2014: 6♀ (1♀ UB); same data, Andricus sp7 (leg. Guo Rui). (8.v.2013) 2013–vi–15: 6♂ (3♂ UB); same data. Andricus sp 8, Z3 (28.iv.2014) 16–v.2014: 9♂ & 8♀ (5♂ & 3♀ UB); same data, (21.iv.2016) 7–9.v.2016: 19♀ (9♀ UB); same data, Dryocosmus sp6 (v.2014) 10.v.2014: 7♂ & 1♀. Qing Liang Feng National Nature Reserve (Zhejiang province, China), 30°30′31.26” N 119°11′59.13”E, on Q. glandulifera var. brevipetiolata ( R. Guo leg), Z1 (10.iv.2013) 8.v.2013: 28♂ (7♂ UB); same data, (iv–2016) 24.iv.2016: 2♀. Changhua (Zhejiang province, China), Q. glandulifera var.brevipetiolata, nº 5131, (8.v.2014) 10.v.2014: 36♂ & 54♀ (10♂ & 15♀ UB); same data, 30°30′31.26” N 119°11′59.13”E, sp 9 ( R. Guo leg), (15.iv.2014) 8.v.2014: 16♂ & 4♀. Qingliang Park (Zhejiang province, China), Q. glandulifera var. brevipetiolata Nakai (Chia Miao-1, Guo Rui leg), (24.iv.2016) iv–v.2016: 22♂ & 54♀ (5♂ & 7♀ UB); same data, (Chia Miao-4, Guo Rui leg), 48♀ (6♀ UB); same data, (Chia Miao-3, Guo Rui leg), (28.iv.2016) iv–v.2016: 73♀ (13♀ UB); same data, (Guo Rui leg), (12.iv.2013) 3.v.2013: 1♀; same data, (28.iv.2016) iv.2016: 1♀. Shouwa, Longgang Town (Lin’an District, Hangzhou City, Zhejiang Province), Q. glandulifera var. brevipetiolata Nakai (Guo Rui leg), in Andricus spp1 series (part), (28.iv.2014) 16.v.2014: 4♀; same data, (v–2014) 10.v.2014: 11♂ & 3♀ (2♂ & 2♀ UB); same data, (15. v.2014) 16.vi.2014: 2♀. Zhuzhou City (Hunan Province), Q. glandulifera var. brevipetiolata Nakai (Zhiwei Liu leg), (8.v.1993) 15.v.1993: 1♀. Shunxi (Zhejiang Province), Q. glandulifera var. brevipetiolata Nakai , (Chia Miao- 2, Rui Guo leg), (29.iv2016) v.2016: 59 (8♀ UB).

Description. SEXUAL FEMALE ( Figs 1–7 ).

Length. Body length 1.2–2.6 mm (n = 25).

Color. Body ambarine or reddish-brown to chestnut. Head usually lighter, sometimes yellowish. Mesosoma with some blackish areas in darker specimens. Metasoma reddish brown, dorsally darker. Antennae light brown; legs brown. Wing veins brown, some pale.

Head ( Figs 1 , 2 c–d). Head transversally quadrangular in front view, alutaceous to coriaceous and shining, with white setae, denser on lower face; 2.0 times broader than long from dorsal view; 1.3 times broader than high and slightly narrower than mesosoma in front view. Lower face weakly alutaceous to smooth, without striae radiating from clypeus, median area slightly elevated. Clypeus trapezoid, slightly broader than high, not incised medially, with projected lamina over mandibles, alutaceous, without elevated rugose central area; anterior tentorial pits large and deep, epistomal sulcus and clypeo-pleurostomal line visible, superficial. Gena alutaceous to delicately coriaceous, indistinctly or slightly broadened behind eye, usually invisible in front view behind eye. Malar space alutaceous to smooth, without malar sulcus, 0.3 times as long as height of eye. Transfacial distance slightly longer than height of eye; inner margins of compound eyes parallel; diameter of antennal toruli 1.7 times larger than distance between them, distance between torulus and inner margin of eye subequal to diameter of torulus. Frons coriaceous, with white setae; interocellar area coriaceous, without rugae. Vertex and occiput uniformly coriaceous, with very weak rugae. POL: LOL: OOL = 6.0: 3.0: 3.0; ocellus rounded, lateral subequal to median ocellus, OOL around 1.6 times diameter of lateral ocellus. Occipital carina absent; postocciput and postgena with delicate longitudinal parallel striae, shining, with setae; posterior tentorial pit large, elongated; height of occipital and oral foramen slightly longer than height of postgenal bridge; hypostomal carina emarginated, incomplete dorsally; gular sulcus absent.

Antennae ( Fig. 2b ) Antenna with 14 segments (rarely with an incomplete suture between F11–F12), slightly shorter than head+mesosoma; F1 1.7 times as long as pedicel (sometimes slightly shorter), around 1.5 times as long as F2 (sometimes shorter), F3 to F10 subequal in length; F12 longer than F11; antennal formula, 12: 9: 16: 11: 11: 12: 12: 12: 12: 11:11: 10: 10: 13. Placodeal sensilla on F2 to F12.

Mesosoma ( Figs 3–4 ). Laterally convex, longer than high in lateral view. Pronotum, mesopleural triangle and metapleuron with uniformly dense white setae. Pronotum rugulose to delicately coriaceous, with alutaceous interspaces between rugae, dorsally smooth and short (around 1/5 lateral length), with some carinae next to mesopleuron. Propleuron weakly alutaceous to smooth, shining, with sparse setae. Mesoscutum as broad as long (width measured across basis of tegulae), smooth and shining, anteriorly coarsely coriaceous to rugose next to notauli, usually with piliferous points; long white sparse setae present along notauli, posterior median area and anteriorly in the sculptured area. Notauli complete, deep posteriorly and superficial in anterior 1/3 of mesoscutum, obscured by sculpture, converging at posterior end; anterior parallel lines faint but present, extending to 1/2 length of mesoscutum; parapsidal lines inconspicuous; median mesoscutal line usually absent, indistinct or superficial, sometimes extending to 1/7 of mesoscutum length. Parascutal carina usually broad, extending to the point where notauli reach pronotum. Transscutal articulation present. Mesoscutellum rounded, as long as broad or very slightly longer, overhanging metanotum, uniformly rugose, with irregular strong rugae, areas between rugae coriaceous, delimited by a carina more or less defined from above. Scutellar foveae transverse, separated by median carina, with smooth shining bottom. Mesopleuron, including speculum, smooth and shining, or with inconspicuous carinae, visible in the centre; mesopleural triangle alutaceous with dense and short white setae anteriorly. Dorsal axillar area reticulated, with smooth areas, and glabrous; mesopleural triangle alutaceous, pubescent; lateral axillar area smooth, with few setae; subaxillular bar smooth, shining. Metapleural sulcus reaching mesopleuron slightly above half of its height, delimiting a relatively narrow or large area ( Fig. 3d and Fig. 3e , respectively), with dense white setae. Metascutellum alutaceous, slightly incised ventrally, with ventral impressed area not visible; metanotal trough weak alutaceous to smooth, shining, with setae in the half-internal area. Lateral propodeal carinae strong, subparallel to divergent anteriorly and bented outwards in the middle, delimiting glabrous rugose central area; lateral propodeal area alutaceous to smooth and shining, with dense long, white setae. Nucha short, alutaceous with longitudinal sulci dorso-laterally and laterally.

Legs. Tarsal segments not shortened (see males), similar to the rest of female gallwasps, ( Figs 5 b–d); tarsal claws toothed, with basal lobe ( Fig. 5b ).

Forewing longer than body ( Fig. 6c ), hyaline, with pubescent surface, margin ciliate; veins dark brown, conspicuous, radial cell long; R1 next to the margin; 2r curved; Rs straight, usually weakly pigmented; radial cell around 3.4 times as long as wide ( Figs 6 d–e), areolet indistinct or absent, only rarely distinct; Rs+M absent, inconspicuous.

Metasoma as long as head+mesosoma or slightly longer, slightly longer than high in lateral view; 2nd metasomal tergite occupying 1/2 of length of metasoma in dorsal view, smooth, shining, with few white setae laterally; all subsequent tergites without setae, micropunctuate, shining ( Fig. 6a ). Prominent part of ventral spine of hypopygium around 4.5 times as long as broad from ventral view, with sparse, white subapical setae, not extending beyond apex of spine ( Fig. 6b ).

MALE. Similar to female except: body length 1.7–2.2 mm (n = 19); uniformly yellowish to amber ( Fig. 7h ) or head yellowish to brown, mesosoma black, metasoma brown, dorsally darker ( Fig. 7i ); antennae and legs light brown; head slightly rounded, around 1.4 times as broad as high in front view ( Fig. 1c ); compound eyes converging basally; diameter of antennal torulus 3.0 times as long as distance between them, distance between torulus and eye margin shorter than diameter of torulus; ocelli rounded, lateral ocellus subequal to median; POL: OOL: OCO = 7:3:3, diameter of ocellus slightly shorter than OOL ( Fig 1d ); antenna ( Fig. 2a ) with 13 flagellomeres, slightly longer than head+mesosoma; pedicel slightly longer than broad, F1 straight, not curved, around 1.7 times as long as pedicel, 1.4 times as long as F2, F3 to F13 subequal in length; antennal formula, 12: 8: 14: 10: 10: 10: 10: 10: 10: 10: 10: 10: 9: 8: 9; placodeal sensilla on all flagellomeres; mesoscutellum slightly longer than broad; mesopleuron, including speculum, completely smooth and shining; in some specimens with few inconspicuous carinae, visible in the central part only; metapleural sulcus reaches mesopleuron in 7/10 of its height, delimiting large area; lateral propodeal carinae diverge, bented basally, sometimes not well defined; radial cell of forewing around 3.3 times as long as wide; areolet absent, if visible than weakly defined; tarsal claws simple; relative length of tarsal segments ( Fig. 5a ) of anterior legs 4.0: 1.5: 1.0: 1.0: 4.0, median legs 3.0: 1.5: 1.5: 1.0: 4.5, and posterior legs: 5.0: 2.0: 1.5: 1.0: 4.0; 2nd metasomal tergite occupying 1/2 of length of metasoma in dorsal view ( Fig. 5a ); subsequent metasomal tergites weakly micropunctuate, sometimes punctures inconspicuous laterally.

Variability. See in Discussion

Gall ( Figs 7 a–g). Galls develop on the axis of male catkins. A single catkin axis can hold 30 to 40 galls, each gall is about 5 mm long and 2–4 mm wide. When the catkin bud opens, the galls develop as a subspherical mass, covered with dense glandular trichomes that give the catkin a spongious aspect ( Fig 7a ). As the catkin axis grows, the galls differentiate into independent cylindrical structures radiating in all directions ( Fig. 7b ). When fresh the galls are green and turn blackish brown as they mature. The cylinders deform into bottle-shaped mature galls, swollen at the base and with a filiform apical appendix, which is usually curved. The individual larval chambers measure around 1mm in diameter. They are located on the swollen base of the gall and up to three chambers may occur in the same gall. The glandular trichomes are deciduous and fall progressively from base to apex. The dry galls are brown and glabrous.

Hosts. Quercus serrata (= Q. glandulifera var. brevipetiolata Nakai (section Quercus of Quercus ). The host, Q. fabri Hance mentioned in Pujade-Villar et al. (2014) and reproduced in Pénzes et al. (2018) is incorrect.

Distribution. China: Hunan, Guizhou and Zhejiang Provinces ( Kieffer 1906, Yang et al. 2012, Wang et al. 2013, Pujade-Villar et al. 2014).

Comments on A. deqingis typical series. According to the material examined section in the original description, the typical series of A. deqingis had 40 paratypes instead of 29 as it is mentioned (16 ♂ & 13 ♀); moreover, the holotype number is also repeated in the paratype series. After examination of the type series by JP-V, the specimens 965063 and 957878 were determined not to be A. deqingus , but are probably undescribed species of Andricus ; specimen 954470 belongs to Synergus ; and the specimens 954474, 957887, 964481, 964482, 964483, 965064, 965065, and 965115 are lost.

Comments on A. flavus typical series. After examination of specimens housed in the ZAFU collection (JP-V), the specimens labelled as ‘holotype’ and ‘paratype’ were determined to have 1.V.2011 as the collection date and 18.V.2011 as the emergence date, and not 8.V.2010 as is published in the original description. The Chinese label was erroneously translated. Additionally, the host was erroneously identified: it is not Q. fabri but Q. glandulifera var. brevipetiolata (Rui Guo, personal communication).

Molecular analyses. The best partition scheme consisted on unlinked GTR+I+G models for each codon position and each mitochondrial gene and a single partition for 28S. The resulting trees presented identical topologies independently of the inference method applied. We summarise the results of the phylogenetic analyses in Fig. 8 . We used the Bayesian tree as a base reference to map the Bayesian and ML supports onto this tree.

We recovered Melikaiella as sister to the rest of genera. The Andricus species were resolved as three clades recovered in a polytomy: (i) the clade of core- Andricus with most of the European, American and Asian species; (ii) a clade encompassing the genera Atrusca , Biorhiza , Cynips , Disholcaspis, Striatoandricus , the Andricus tecturnarum species-group, and A. quercuslanigera ; (iii) a small clade formed by the European species Andricus inflator , and A. hakonensis in Asia.

In the core- Andricus clade, the Asian species formed a well-supported sister clade to the rest of Andricus (American and European species). The clade comprising the Asian Andricus also included the ‘ Parandricus group’, now delimited as Andricus mairei ( Fig. 8 ).

Within the core- Andricus group of species, interspecific uncorrected genetic distances ranged from 4 to 14.3%, while intraspecific distances were usually below 2% ( Table 2). In the case of our revised delimitation for Andricus mairei , most of the analysed specimens show distance values below 1%. However, the specimen A. mairei _ILV91 showed pairwise divergence with the remaining species in the group ranging from 6 to 7%.

Figures

FIGURE 1. Andricus mairei head: (a) female, front view, (b) female, dorsal view, (c) male, front view, (b) male, dorsal view.

FIGURE 2. Andricus mairei: (a) antenna, male, (b) antenna, female, (c) head, female, posterior view, (d) female, malar space.

FIGURE 3. Andricus mairei, mesosoma: (a, b, f) dorsal view, (c–e) lateral view.

FIGURE 4. Andricus mairei: a–d, variability of propodeum structures.

FIGURE 5. Andricus mairei: (a) male legs with details of tarsal claws (L=leg), (b–d) female legs with details of tarsal claws.

FIGURE 6. Andricus mairei: (a) female metasoma, lateral view, with details of micropuncture, (b) female, ventral spine of hypopygium, (c) female, dorsal view, (d–e) radial cell of forewing.

FIGURE 7. Andricus mairei: (a–d) young galls, (e) old galls, (f) details of galls in transverse section, (g) one single gall, (h–i) chromatic variability in males.

FIGURE 8. Bayesian phylogenetic tree of Cynipini using three concatenated molecular markers (COI, cytb, and 28S). Node supports are posterior probabilities. Dryocosmus cerriphilus and Dryocosmus kuriphilus are used to root the tree. New synonyms of Andricus mairei (Andricus flavus n. syn. and Andricus deqingis n. syn.) are indicated. Explanation in the text.