Andricus forni Pujade-Villar & Nicholls, 2020

Pujade-Villar, Juli, Wang, Yiping, Cuesta-Porta, Víctor, Guo, Rui, Nicholls, James A. & Melika, George, 2020, Andricus forni Pujade-Villar & Nicholls n. sp., a new species of oak gallwasp from China (Hymenoptera: Cynipidae), Zootaxa 4890 (4), pp. 554-566 : 555-562

Andricus forni Pujade-Villar & Nicholls n. sp.

urn:lsid:zoobank.org:act:C88FE778-168B-4094-BAC4-881F3D88AE7E

( Figs 1–5 )

Type material. HOLOTYPE ♀: “ Tianmushan, Lin’an District, Hangzhou City , Zhejiang Province ” (white label); Q. glandulifera , (24.iv.2011) 27.iv.2011 (leg. Rui Guo) (white label); “ Holotype ♀, Andricus forni n. sp. (desig. J. P-V)” (red label) . Holotype is deposited at UB (JP-V col.) . Paratypes: 40³ & 40♀ (20³ & 20♀ at UB; 20³ & 20♀ at ZAFU) with the same labels as holotype .

Additional material examined. Same data as holotype, 91³ & 37♀ (14³ & 10♀ UB, remainder at ZAFU). Tianmushan, Lin’an District , Hangzhou City , Zhejiang Province, Q. glandulifera (24.iv.2011) 25.iv..2011: 10³ & 7♀ (previously labeled as “ Dryocosmus spp10” and D. fabri in litt. det Wang). Kaishan Old Hall Attractions in Tianmu Mountain , Zhejiang Province, 11.v.1999: 1♀. Elephant Trunk Hill, Lin’an, Hangzhou City, Zhejuang Province, ex Q. glandulífera var. brevipetiolata Nakai, Shijun Wang leg. (6.iv.2013) 23.iv.2013: 4³ & 9♀ (previ-ously labeled as “ Dryocosmus spp4” det Wang); same data (5.iv.2014) 28.iv.2014: 1³ & 22♀; same data (6.iv.2013) 23–26.iv.2013: 2♀; (23.iv.2013) 6.v.2013: 1♀. Changhua Town, Lin’an District , Hangzhou City, Zhejiang Province, Q. glandulifera , (12.iv.2013) 16.v.2014: 4♀ (previously labeled as “ Dryocosmus spp8” det Wang; the emergence date is a mistake, it should be 2013). Qingliangfeng, Lin’an District , Hangzhou City, Zhejiang Province, Q. glandulifera , (12.iv.2013) 2.v.2013: 1♀ (leg Jie, sample code 5132), 2♀ used for DNA; 21.iv.2015: 1♀ (leg. Jie 6191). Xiangbishan Lin’an District , Hangzhou City, Zhejiang Province, Q. glandulifera , (6.iv.2014) 23.iv.2014: 2♀ (leg. Jie, sample codes 5261, 5134) .

Diagnosis. Andricus forni n. sp. most closely resembles A. xishuangbannaus and A. moriokae by having the head anteriorly black, except on and around clypeus which is brown; malar space with striae; female antenna with F1 at most 1.2x as long as F2 while male antenna with last flagellomere at most 2.0x as long as broad and F1 slightly curved and not swollen apically; mesoscutum completely smooth or delicately alutaceous to smooth, only with very few setae along notauli and in the lateral corners;prominent part of the ventral spine of the hypopygium at most 4.0x as long as broad. In A. forni n. sp., lower face dark and strongly alutaceous to coriaceous, frons alutaceous, in females POL1.6x OOL, in males 2.0x OOL; female antenna with 12 flagellomeres (sometimes the suture between F11–F12 is incomplete but always visible), radial cell 3.5x as long as broad, central and lateral propodeal areas smooth, without wrinkles or rugae; lateral propodeal carinae complete, curved outwards posteriorly; galls on Q. serrata . In A. xishuangbannaus , only females are known, lower face light brown, smooth and shiny; frons smooth and shiny; central propodeal area with some irregular wrinkles and rugae, lateral propodeal area rugose, galls on Q. griffithii . Finally, Andricus moriokae differs from A. forni n. sp. by having a shorter POL in females (around 1.3x OOL), female antenna with 11 flagellomeres, the radial cell longer (4.1x as long as broad) and, in males, the lateral propodeal carinae are incomplete basally (ending at the level of dorsal propodeal margin).

Etymology. Named after Mr. Joaquim Forn i Chiariello.

Description.

FEMALE. Body length 1.1–2.0 mm, n = 21.

Color. Head, mesosoma and metasoma entirely and uniformly very dark brown to black; clypeus and mandibles brown, usually lighter than the rest of lower head ( Fig. 5b ); antenna light brown, last flagellomeres sometimes slightly darker; maxillary and labial palpi light yellow; tegula light brown; legs uniformly light brown, with coxae slightly darker at the base; ventral spine of hypopygium brown.

Head ( Fig. 1a, 1c, 1d ) smooth, with sparse white setae on lower face; 2.0x broader than long in dorsal view, 1.3x broader than high and slightly broader than mesosoma in anterior view. Clypeus trapezoid, emarginate, with a weak median incision ventrally, weakly alutaceous, with some setae; anterior tentorial pits, epistomal sulcus and clypeo-pleurostomal line distinct, deep. Gena delicately alutaceous, not broadened behind eye, as long as diameter of eye in lateral view; malar space with delicate striae extending towards compound eye without reaching margin of eye, 0.3x shorter than height of eye. Compound eyes slightly convergent ventrally. Transfacial distance only 1.3x wider than height of eye; diameter of antennal toruli greater than distance between them, distance between torulus and inner margin of eye nearly equal to diameter of torulus; lower face, including slightly elevated median area, delicately coriaceous to alutaceous, with white setae. Frons and vertex delicately alutaceous, with few setae; interocellar area and occiput coriaceous. POL 1.6x broader than OOL; OOL 1.1–1.3x longer than LOL and around 2.0x longer than length of lateral ocellus; all ocelli of same size and shape. Postocciput and postgena smooth, shiny, without setae; posterior tentorial pit large, deep, the area below impressed; height of occipital foramen nearly equal to height of postgenal bridge; hypostomal carina emarginate, continuing into postgenal sulcus.

Antenna ( Fig. 2 a–b) with 12 flagellomeres, F11 longer than F12 (suture between F12 and F11 rarely incomplete); 1.3x longer than head+mesosoma; pedicel longer than broad; F1 around 1.1x longer than F2, 1.9x longer than pedicel; F2–F12 progressively shorter; placodeal sensilla on F2–F12, absent on F1. Antennal formula: 15: 12(x10): 23: 20: 17: 17: 16: 16: 15: 15: 15: 13: 12: 18.

Mesosoma ( Fig. 3 a–c) 1.15x longer than high. Pronotum smooth, shiny, with delicate parallel striae and dense white setae laterally; propleuron shiny, alutaceous to smooth anteriorly, with delicately coriaceous central and basal area. Mesoscutum smooth, shiny, with some white setae in the anterior corners and beside notauli; 1.2x wider than long (greatest width measured across mesoscutum at level of base of tegulae). Notauli complete, deep, slightly converging at the posterior end; anterior parallel, parapsidal, median mesoscutal lines absent; parascutal carina reaching notauli. Mesoscutellum rectangular, uniformly dull rugose to coriaceous, as long as broad, overhanging metanotum; circumscutelar carina usually well impressed; scutellar foveae distinct, transversely ovate, narrow, with smooth and shining bottom, with a very short coriaceous median carina separating foveae. Mesopleuron and speculum smooth, shiny, without setae except for dense patch of setae on posteroventral quarter of mesopleuron, with few impressed foveae along acetabular carina; dorsal axillar area smooth, shiny; axillula with dense white setae; lateral axillar area coriaceous, without setae, sometimes with a few rugae; subaxillular bar triangular, smooth, shiny, most posterior part broader than height of metanotal trough; metapleural sulcus reaching mesopleuron at almost half of its height. Metascutellum uniformly rugose-carinated, metanotal trough smooth, shiny, with dense short white setae; ventral impressed area shorter than height of metascutellum, smooth; central propodeal area smooth, shiny; lateral propodeal carinae strong, curved outwards in posterior third; lateral propodeal area smooth, rarely alutaceous, with a single ruga next to spiracle, with dense long white setae. Nucha with irregular wrinkles and rugae.

Legs with tarsal claws with basal lobe.

Forewing ( Fig. 5a ) longer than body, hyaline, with distinct long, dense cilia on margin, radial cell 3.5x longer than wide; R1 reaching wing margin, Rs nearly straight, reaching wing margin; areolet small, triangular, closed and distinct. Rs+M distinct at two-thirds of distance to basalis and its projection reaching basalis at mid-height.

Metasoma ( Fig. 4a ) shorter than head+mesosoma, higher than long in lateral view; second metasomal tergite occupying more than half of metasoma in dorsal view, with some white setae laterally, all subsequent tergites without setae, smooth, shiny, with very delicate micropunctures. Hypopygium with micropunctures, ventral spine of hypopygium relatively short, prominent part 4.0x longer than broad, with two parallel rows of white setae ventrally.

MALE ( Figs. 1b, 1d, 1f , 2c , 3d , 4b ). Similar to female except for: clypeus with the same color as lower face (rarely lighter); middle of last femur and last tibia also slightly darker; malar space around 0.2x as long as height of eye; transfacial distance around 1.1x wider than height of eye; gena 0.5x shorter than cross diameter of eye in lateral view; POL about 1.9x broader than OOL; OOL subequal in length to lateral ocellus, and 1.3x longer than LOL; central ocellus smaller; antenna with 15 flagellomeres; pedicel as long as broad; F1 very slightly curved and not swollen apically, 1.3–1.4x longer than F2, 2.5–2.6x longer than pedicel and 3.8-4.3x as long as its narrowest width; F3–F12 subequal in length; F1–F6 slightly wider than the remainder of flagellomeres; placodeal sensilla on all flagellomeres; antennal formula: 10: 8(x8): 21: 15: 14: 14: 13: 13: 13. 13: 12: 12(x7): 12: 11: 15. Body length 1.0– 1.6 mm, n = 15

Gall. The gall ( Fig. 5c ) is integral to the leaf blade, occurring singularly, never in clusters, without a distinct internal larval chamber. The gall is approximately spherical, 2.6–3.1 mm in height (n=6), and the outer gall tissues protrude equally on both sides of the leaf lamina.Young galls are fleshy, yellowish to green, turning dry and dark brown after emergence of the adult wasps.

Biology. Only the sexual generation is known, inducing galls on Q. serrata . Mature galls were collected in mid-April, adults emerge from mid-April to May.

Distribution. Currently known only from Zhejiang Province, China. Probably distributed all over the range of its host plant. The host is native to southern, central and eastern China, also in Taiwan, Japan and Korea from 100 to 2000 m a.s.l. ( Huang et al., 1999).

After a thorough examination of specimens and original descriptions of A. pseudocurvator , A. songshui , A. formosanus and A. moriokae , the descriptions of A. mukaigawae , A. wuhanensis and A. xishuangbannaus , the redescription of A. moriokae , and additional literature mentioned in the discussion, we propose the following key to differentiate the sexual generations of the valid Andricus species obtained from small spherical integral leaf galls on oaks in the Eastern Palaearctic and Oriental Regions. We also note the host oaks galled by each Andricus species.

1 Anterior half of mesoscutum distinctly sculptured, strongly alutaceous to coriaceous....................... A. songshui [ Q. serrata ]

- Mesoscutum completely smooth or with a very delicate alutaceous or imbricate sculpture mainly in the anterior corners.... 2

2 Mesoscutum obscurely imbricate with scattered hairs all over mesoscutum. Female F1 about 1.4x longer than F2................................................................................................. A. mukaigawae [ Q. serrata , Q. mongolica var grosseserrata , Q. dentata ]

- Mesoscutum smooth or delicately alutaceous, with a few setae only along notauli and in the lateral corners, with glabrous areas. Female F1 shorter, at most 1.2x longer than F2.............................................................. 3

3 Females ............................................................................................. 4

- Males.............................................................................................. 9

4 Prominent part of ventral spine of hypopygium at least 6.0x longer than broad..................................... 5

- Prominent part of ventral spine of hypopygium at most 4.0x longer than broad..................................... 6

5 Antenna with 11 flagellomeres (but the last sometimes with an indistinct suture, so appears as 12 flagellomeres); central propodeal area without or with few irregular delicate wrinkles........................................ A. pseudocurvator [ Q. serrata , Q. fabrei ]

- Antenna with 11 flagellomeres; central propodeal area with irregular wrinkles.......................... A. wuhanensis [ Q. fabrei ]

6 Head brown anteriorly, especially lower face; malar space without striae, frons with distinct alutaceous sculpture.................................................................................................. A. formosanus [ Q. dentata ]

- Head black anteriorly, any brown restricted to clypeus and around clypeus, malar space with striae; frons smooth, shiny or very delicately sculptured................................................................................... 7

7 Lower face and frons smooth and shiny; central propodeal area with some irregular wrinkles and rugae, lateral propodeal area rugose.............................................................................. A. xishuangbannaus

[ Q. griffithii ]

- Lower face and frons delicately alutaceous to coriaceous; central and lateral propodeal area smooth, without wrinkles and rugae............................................................................................... 8

8 POL about 1.6x as long as OOL; antenna with 12 flagellomeres, sometimes the suture between F11-F12 is incomplete; radial cell 3.5x as long as broad..................................................................... A. forni n. sp. [ Q. serrata ]

- POL only 1.3x as long as OOL; antenna always with 11 flagellomeres, never with suture in F11; radial cell 4.1x as long as broad..................................................................................... A. moriokae [ Q. serrata ]

9 Last flagellomere more than 2x as long as broad............................................... A. pseudocurvator [ Q. serrata , Q. fabrei ]

- Last flagellomere at most 2.0x as long as broad............................................................. 9

10 F1 apically swollen; body brown.............................................................. A. formosanus [ Q. dentata ]

- F1 more cylindrical, very slightly curved and not swollen apically; body predominantly black....................... 10

11 POL around 2x as long as OOL; lateral propodeal carinae complete, curved outwards in posterior third....... A. forni n. sp. [ Q. serrata ]

- POL around 1.6x as long as OOL; lateral propodeal carinae diverging ventrally and incomplete or inconspicuous basally, ending at level of dorsal propodeal margin........................................................... A. moriokae [ Q. serrata ]

The cytb tree of Asian Andricus contains four major clades indicated with A–D in Fig. 6 . Major clades A, C and D contain species with sexual generations inducing integral leaf galls. The species A. mukaigawae is recovered as monphyletic in a well-supported node, sister to the terminals of A. kashiwaphilus and A. pseudoflos , albeit the internal relationships between these two species is not well resolved. The new species, A. forni , is recovered as monophyletic within the clade C, closely allied to A. xishuangbannaus , A. moriokae , A. pseudocurvator and A. formosanus , as is also suggested by the morphological similarity of A. forni with this group, in particular with the first two species. Within this group, A. formosanus is the most phylogenetically distinct, while the remaining four form a genetically close complex of species. However, these four still show divergence consistent with being discrete species; for example the new species A. forni is 1.7–2.5% divergent from the other three species, within the range observed for other distinct cynipid species ( Nicholls et al., 2018; Nicholls & Pujade-Villar, 2020). Finally, the species A. hakonensis and A. songshui are recovered within the clade D, which is sister to the rest of Andricus species, albeit the relationships between these two species is unclear. All new sequences are deposited in GenBank, accessions MT922013 – MT922034 .

Figures

FIGURE 1. Head of Andricus forni n. sp.: (a) female in frontal view, (b) male in frontal view, (c) female in dorsal view, (d) male in dorsal view, (e) female in posterior view, (f) male in posterior view.

FIGURE 2. Andricus forni n. sp., antennae: (a) female antenna with detail of last flagellomeres, F11 and F12 completely separated, b) female antenna with detail of last flagellomeres, F11 and F12 incompletely separated, (c) male with detail of F1.

FIGURE 3. Andricus forni n. sp., mesosoma: (a) female in dorsal view, (b) female in lateral view, (c) female propodeum, (d) male propodeum.

FIGURE 4. Andricus forni n. sp., metasoma and details of micropunctures: (a) female, (b) male.

FIGURE 5. Andricus forni n. sp.: (a) forewing, (b) frontal head of female with clear area around clypeus, (c) galls with details.

FIGURE 6. Bayesian majority-rule consensus tree of 433bp of cytochrome b sequence derived from Asian Andricus species. Numbers at nodes indicate posterior probability support; major clades mentioned in the text are indicated by the letters A–D.