Neuroterus niger Gillette, 1888

Nicholls, James A., Melika, George, Digweed, Scott C. & Stone, Graham N., 2022, Pairing of sexual and asexual generations of Nearctic oak gallwasps, with new synonyms and new species names (Hymenoptera: Cynipidae, Cynipini), Zootaxa 5145 (1), pp. 1-79 : 48-56

Neuroterus niger Gillette, 1888

Figs 151–182

Synonyms: Neuroterus nigrum Gillette (1888: 218) , females and galls. Revised spelling by Dalla Torre and Kieffer (1902: 51).

Neuroterus papillosus Beutenmueller, 1910 , syn. nov.

Neuroterus perminimus Bassett, 1900 . Synonymized by Beutenmueller (1910: 121), and treated as a variety of N. niger by Kinsey (1923: 48), but synonymy ignored by Weld (1951) and later authors; syn. nov.

Neuroterus vernus Gillette, 1889 , sexual generation, syn. nov.

Kinsey (1923) described 5 additional varieties of N. niger , all inducing integral leaf galls. Four we consider as synonyms: Neuroterus niger var. arizonicae Kinsey, 1923 (asexual generation, Arizona, on Q. arizonica ), syn. nov.; Neuroterus niger var. grisea Kinsey, 1923 (asexual generation, Texas, on Q. grisea ), syn. nov.; Neuroterus niger var. nigripes Kinsey, 1923 (asexual generation, Texas, on Q. sinuata var. breviloba (= Q. breviloba ) and Q. stellata ), syn. nov.; Neuroterus niger var. pattersoni Kinsey, 1923 (asexual and sexual generations, Texas, on Q. sinuata var. breviloba (= Q. breviloba ) and Q. stellata , respectively), syn. nov. .

The fifth variety described by Kinsey is Neuroterus niger var. alimas Kinsey, 1923 (sexual generation, Texas, on Q. virginiana ) that was still considered as form of N. niger by Burks (1979). According to Kinsey (1923) this variety induces a sexual generation spring gall, while the other four varieties induce autumn asexual generation galls. Moreover, N. niger var. alimas is the only variety associated with section Virentes oaks while the other four are on section Quercus oaks, and as mentioned in the Introduction, no Nearctic cynipid species are shared across the oak sections ( Abrahamson et al. 1998 a, 2003; Stone et al. 2009). Hence biological information suggests that N. niger var. alimas is a species distinct from N. niger (sensu Gillette 1888) and the other four of Kinsey’s varieties. Kinsey (1923) described N. niger var. alimas based on one female (holotype – lost) and 13 males and gave no detailed morphological description for this variety. Thus, there is no morphological evidence for synonymisation of N. niger var. alimas to N. niger while at the same time it cannot be treated as a valid species so Melika et al. (2021) moved it to nomen dubium.

Types examined. Asexual generation of Neuroterus niger Gillette : one female labelled as “Ac. Cat. 851”, “Ag. Coll. Michigan 3-25-88”, red label “Type No 1898 USNM”, handwritten “ N. nigrum ”. Neuroterus niger var. alimas Kinsey, 1923 : holotype female labelled as “Acc.24856”, pink ” N. alimas , female, Holo- Paratype ”, ” Q. virginiana ”, ”Austin, Tex. 4.16.21., Patterson” – insect absent, only gall. Neuroterus niger var. arizonicae Kinsey, 1923 : holotype female labelled as ”Ac. 24856”, pink ” N. arizonica , Holo- Paratype’, ” Q. arizonica, Kinsey coll.”, ”Bisbee, Ariz. Gall 1.15.20.” – insect absent, only gall. Neuroterus niger var. griseae Kinsey, 1923 : holotype female labelled as ”Ac. 24856”, pink ” N. griseae , Holo-Paratype’, ” Q. grisea, Kinsey coll.”, ”Fort Davis, Tex., Gall. 12.16.19.” – insect absent, only gall. Neuroterus niger var. nigripes Kinsey, 1923 : holotype female labelled as ”Ac. 24856.”, pink ” Neuroterus nigripes , Holo- Paratype’, ” Q. stellata, Kinsey coll.”, ”Austin, Tex. 12.4.19.” Neuroterus niger var. pattersoni f. pattersoni Kinsey, 1923 : holotype female labelled as ”Ac. 24856.”, pink ” Neuroterus pattersoni , Holo- Paratype’, ” Q. stellata, Patterson coll.”, ”Austin, Tex. 5.7.21., gall 310. 21.” Sexual generation of Neuroterus niger : 3 females on one pin “Io”, “Ac. Cat. 996”, red label “Type”, handwritten label “ Neuroterus vernus Gill. ”; 5 females on one pin: handwritten label “ Iowa, Gillette”, white label “Type”, “colCF Baker”; also one label with galls and red label “Type”. Neuroterus papillosus Beutenmueller, 1910 : two females on two pins, both labelled as “Bronx Park, New York City, W. Beutenmüller”, red label “Type”, “Beut. Coll. rec’d 1935”, handwritten label “ Neuroterus papillosus Beutnm ”. Types were examined by GM during his multiple visits to the AMNH, NYC and USNM, Washington, DC.

Material examined. Five asexual females labelled as “ CANADA: Alberta, Edmonton, Grand Trunk Pool, SC30, 2002.04.12. S. Digweed, Neuroterus niger Gillette females of the asexual generation, det. S. Digweed 2005”. Sexual generation: 5 females labelled as “ CANADA, Alberta, Edmonton. Reared 18.iv.2005, ex Q. macrocarpa . N. niger (?) gall, Grand Trunk, coll.22.ix.04. S. Digweed ”; 5 males labelled as “ CANADA, Alberta, Edmonton. Reared 3-13.x.2005, ex Q. macrocarpa . N. niger (?) gall, Grand Trunk, coll.22.ix.04. S. Digweed ”. Specimens have been deposited at the USNM, PHDNRL and RAM . Asexual females have been deposited at the PHDNRL and RAM.

Diagnosis. Belongs to Kinsey’s (1923) subgenus Diplobius . The oak gallwasp ( Cynipini ) fauna of the Nearctic north of Mexico is divided into three geographic zones, with distinct species: the eastern United States ( Weld 1959), the US Southwest ( Weld 1960) and the Pacific Slope ( Weld 1957). In the eastern US four species, including N. niger , induce parenchyma thickening integral leaf galls; however, the three other Neuroterus species are all only known from their sexual generations. Neuroterus fugiens Weld, 1926 , induces galls on Q. macrocarpa in spring in Illinois, USA; N. papillosus Beutenmueller, 1910 , induces galls on Q. bicolor in USA: NY, NJ, IN, IL; N. perminimus Bassett, 1900 , induces galls on Q. alba in USA: NY, MD, VA, OH, IL and Canada: ON ( Burks 1979). Galls of N. fugiens are quite different, being covered in rose-red hairs on their lower surface and not emerging from the upper leaf surface ( Weld 1926). However, the galls of N. papillosus are the same as in the sexual generation of N. niger designated herein. Kinsey (1923) treated N. papillosus as Neuroterus niger var. papillosus and N. perminimus as N. niger var. perminimus and our assessment of morphology supports this synonymy. Below the descriptions of the asexual and sexual females and males are given according to the current morpho-description requirements (the original descriptions by Gillette (1888, 1889) are very superficial).

Description. Asexual female ( Figs 151–161 ). Body, antenna, legs uniformly dark brown.

Head alutaceous, with sparse white setae, denser on lower face; strongly transverse, 1.3× as broad as high and broader than mesosoma in frontal view, 1.9× as broad as long in dorsal view. Gena alutaceous, broadened behind eye in frontal view, just over half as wide as transverse diameter of eye in lateral view. Malar space alutaceous, with malar sulcus, eye 3.8× as high as height of malar space. Inner margins of eyes parallel. POL 1.8× as long as OOL; OOL 2.1× as long as diameter of lateral ocellus and as long as LOL; all ocelli slightly ovate, of same size. Transfacial distance 1.2× as long as height of eye; diameter of antennal torulus slightly longer than distance between them, distance between torulus and eye 1.3× as long as diameter of torulus. Lower face and median elevated area alutaceous, with white setae, without striae. Clypeus rectangular, 1.8× as broad as high, alutaceous, with long setae along ventral edge; ventrally not emarginate, without median incision; anterior tentorial pit small, rounded, indistinct; epistomal sulcus and clypeo-pleurostomal line impressed, distinct. Frons and interocellar area alutaceous, without setae. Vertex, occiput, postocciput, postgena alutaceous; posterior tentorial pit large, ovate, area below impressed; occipital foramen shorter than height of postgenal bridge; hypostomal carina emarginate, continuing into postgenal sulci which are widely spaced, only slightly diverge toward occipital foramen, postgenal bridge anteriorly only slightly broader than high. Antenna longer than head+ mesosoma, with 10 flagellomeres, pedicel 1.8× as long as broad, F1 1.2× as long as pedicel and 1.4x as long as F2, F2=F3, F4 slightly longer than F3, F5 shorter than F4 and shorter than F6, F7 to F9 gradually shorter until F9; F10 2.0× as long as F9 (F10 probably consists of two flagellomeres, with invisible suture between two flagellomeres); placodeal sensilla on F5–F10.

Mesosoma as long as high. Pronotum smooth, polished, glabrous, without setae in frontal view; alutaceous laterally; propleuron smooth, glabrous. Mesoscutum smooth, glabrous, with setae only along sides; as long as broad (greatest width measured across mesoscutum level with base of tegulae). Notaulus, anterior parallel line, median mesoscutal line and parapsidal line absent; circumscutellar carina narrow present. Transscutal articulation absent, mesoscutum fused with mesoscutellum; as a result of fusion of the mesoscutum and mesoscutellum, the boundary between these structures is not straight but slightly curved towards the mesoscutum; the mesoscutum is emarginate posterolaterally and slightly elevated above the dorsoaxillar area. Mesoscutellum nearly as broad as long, posteriorly rounded, uniformly smooth, glabrous, without setae, overhanging metanotum; mesoscutellar foveae absent. Mesopleuron with speculum and mesopleural triangle uniformly alutaceous, without setae; transverse impressed line present in ventral 1/4 of height of mesopleuron; dorsal and lateral axillar areas alutaceous, without setae; subaxillular bar smooth, glabrous, at posterior end as high as height of metanotal trough; metapleural sulcus reaching mesopleuron slightly below half its height, delimiting narrow smooth area along mesopleuron. Metascutellum smooth, as high as height of smooth, glabrous ventral impressed area; metanotal trough smooth, glabrous, without setae; propodeum smooth, glabrous; central propodeal area smooth, glabrous, with some longitudinal interrupted rugae; lateral propodeal carinae absent; lateral propodeal area smooth, glabrous, without setae. Nucha short, smooth, without sulci. Tarsal claws simple, without basal lobe.

Forewing longer than body, hyaline, margin with dense long cilia, veins dark brown, radial cell open, 5.0× as long as broad; R1 nearly reaching wing margin, Rs reaching wing margin; areolet large, triangular, indistinct, Rs+M light brown, visible along 1/3 of its length, projection reaching basalis in the lower 1/3 of its height.

Metasoma slightly longer than head+mesosoma, nearly as long as high in lateral view; all terga weakly sclerotized, thus limits of terga hardly visible. 2nd metasomal tergum extending to half the length of metasoma in dorsal view, without setae; all terga smooth, glabrous, without micropunctures. Hypopygium without micropunctures, prominent part of ventral spine of hypopygium short, greater than 2.0× as long as broad in ventral view, without setae ventrally. Body length 1.4–1.5 mm (n = 3).

Sexual female (= N. vernus ) ( Figs 162–166 , 172–177 ). Body, antenna, legs uniformly reddish brown.

Head alutaceous, with sparse white setae on lower face; transverse, 1.3× as broad as high and broader than mesosoma in frontal view, 2.0× as broad as long in dorsal view. Gena alutaceous, slightly broadened behind eye in frontal view, narrower than transverse diameter of eye in lateral view. Malar space alutaceous, with malar sulcus in the form of a deep impressed stripe; eye 4.5× as high as height of malar space. Inner margins of eyes parallel. POL 2.5× as long as OOL; OOL 1.4× as long as diameter of lateral ocellus and as slightly shorter than LOL; all ocelli ovate, of same size. Transfacial distance 1.2× as long as height of eye; diameter of antennal torulus slightly longer than distance between them, distance between torulus and eye 1.5× as long as diameter of torulus. Lower face and median elevated area alutaceous, without setae and striae. Clypeus rounded, as long as broad, alutaceous, with a few setae scattered all over; ventrally rounded, not emarginate, without median incision; anterior tentorial pit large, rounded, distinct; epistomal sulcus and clypeo-pleurostomal line impressed, distinct. Frons and interocellar area alutaceous, without setae; area under frontal ocellus impressed, alutaceous. Vertex, occiput, postocciput, postgena alutaceous; posterior tentorial pit large, ovate, area below impressed; occipital foramen shorter than height of postgenal bridge; hypostomal carina emarginate, continuing into postgenal sulci which are widely spaced and only diverge slightly toward occipital foramen, postgenal bridge anteriorly only slightly broader than high. Antenna longer than head+ mesosoma, with 11 flagellomeres, pedicel 1.6× as long as broad, F1 1.5× as long as pedicel and 1.6× as long as F2, F2=F3, F4 slightly longer than F3 and equal F5 and F6, all subsequent flagellomeres slightly shorter than F6 and all equal in length; placodeal sensilla on F2–F11.

Mesosoma as long as high. Pronotum alutaceous, with a few setae in frontal view; alutaceous laterally; propleuron alutaceous. Mesoscutum smooth, glabrous, with setae only along sides; as long as broad (greatest width measured across mesoscutum level with base of tegulae). Notaulus, anterior parallel line, median mesoscutal line and parapsidal line absent; circumscutellar carina narrow present. Transscutal articulation absent, mesoscutum fused with mesoscutellum; as a result of fusion of the mesoscutum and mesoscutellum, the boundary between these structures is not straight but slightly curved towards the mesoscutum; the mesoscutum is emarginate posterolaterally and slightly elevated above the dorsoaxillar area. Mesoscutellum nearly as broad as long, posteriorly rounded, uniformly smooth, glabrous, without setae, overhanging metanotum; mesoscutellar foveae absent. Mesopleuron and mesopleural triangle uniformly alutaceous, without setae; speculum smooth, glabrous; transverse impressed line present in ventral 1/4 of height of mesopleuron, extending across entire width of mesopleuron; dorsal and lateral axillar areas alutaceous, without setae; subaxillular bar smooth, glabrous, at posterior end as high as height of metanotal trough; metapleural sulcus reaching mesopleuron slightly below half its height, delimiting narrow smooth area along mesopleuron. Metascutellum smooth, 3.0× as high as height of smooth, glabrous ventral impressed area; metanotal trough smooth, glabrous, without setae; propodeum smooth, glabrous; central propodeal area coriaceous, with longitudinal interrupted rugae; lateral propodeal carinae absent; lateral propodeal area smooth, glabrous, without setae. Nucha short, smooth, without sulci. Tarsal claws simple, without basal lobe.

Forewing longer than body, hyaline, margin with dense long cilia, veins light brown, radial cell open, 5.0× as long as broad; R1 and Rs reaching wing margin; areolet small, triangular, indistinct, Rs+M light brown, visible along 2/3 of its length, projection reaching basalis slightly below its mid height.

Metasoma as long as head+mesosoma, nearly as long as high in lateral view; all terga weakly sclerotized, thus limits of terga hardly visible. 2nd metasomal tergum extending to half the length of metasoma in dorsal view, without setae; all terga smooth, glabrous, without micropunctures. Hypopygium without micropunctures, prominent part of ventral spine of hypopygium short, as long as broad in ventral view, without setae ventrally. Body length 1.4–1.6 mm (n = 4).

Male ( Figs 167–171 , 178–180 ). Similar to female, body brown, antenna and legs slightly lighter; ocelli bigger than in female. Body length 0.9–1.4 mm (n = 5). Originally Gillette (1889) described only females, no males were observed or reared.

Gall. The asexual generation gall is described by Gillette (1888) and are small blisters integral to the leaf blade ( Fig. 181 ). The sexual generation galls ( Fig. 182 ), first recorded as N. vernus , are cells hidden within new shoots, on the young leaf petioles and midribs and on the catkins of Q. macrocarpa ; these plant organs are sometimes distorted as a result ( Digweed 2010).

Biology. See Gillette (1890), Beutenmueller (1910), Kinsey (1923), and Weld (1926) for the biology of one or both generations. The minute, integral leaf galls of the asexual generation have been recorded on Q. macrocarpa . Galls became evident in Edmonton in August and matured in September. This species represents a rare case where males are present in the asexual generation. Males of the asexual generation comprised a tiny fraction of the cynipids reared from asexual generation galls, with only 62 males reared from gall collections made in Edmonton during 2004- 2006, as opposed to 20979 females. In addition, most males were reared in the autumn (October-December) of the year of gall formation, whereas almost all females emerged in April-May the following spring after gall formation. Thus, most males were temporally isolated from ovipositing females and therefore essentially functionless. This is similar to Patterson’s (1928) discovery of functionless males of the asexual generations of Neuroterus contortus ( Weld, 1921) and N. quercusrileyi (Bassett, 1881) . In his study, males and females co-occurred, but they appeared unwilling to mate under laboratory conditions.

Galls of the sexual generation are on Q. alba , Q. bicolor and Q. macrocarpa ( Gillette 1890, Burks 1979, Digweed 2010). We observed that clusters of galls (e.g., on one catkin) often produced adults of only one gender. Galls were visible in Edmonton in May, with adults emerging in late May or early June. Sexual generation females were observed ovipositing mostly on the undersides of leaves and often on leaves that were on long shoots and/or that were not yet fully mature.

Distribution. In the USA the asexual generation has been recorded from Massachusetts, Michigan, Wisconsin, Iowa ( Burks 1979), Illinois, Indiana, New York, New Jersey, Pennsylvania, Ohio ( Beutenmueller 1910); Arizona, Texas ( Kinsey 1923), and Alberta and Manitoba in Canada. The sexual generation has been recorded from Illinois ( Weld 1926), Iowa ( Burks 1979), and TX ( Kinsey 1923) in the USA and Alberta in Canada.

Molecular taxonomy. Alternating generations of this species, which have been previously described under different names ( Digweed 2010), were matched using DNA data from four individuals (two asexual females, two sexual females) sequenced for both cytb and ITS2. Cytb sequences were identical among the four individuals (GenBank accessions OM321646 – OM321649 ), as were ITS2 sequences ( OM331835 – OM331838 ).

Comments. In the Southwest of the USA (AZ, UT) one species, N. howertoni Bassett, 1890 asexual generation, is known to induce leaf parenchyma thickening galls on Q. arizonica and Q. oblongifolia which are like those of N. niger ( Weld 1960) , while in California there is another species, N. engelmannii Kinsey, 1922 , which induces similar galls on Q. engelmannii ( Kinsey 1922 a, 1923; Weld 1957).

Figures

FIGURES 151–156. Neuroterus niger Gillette, asexual generation, female. 151–154, head: 151, frontal view, 152, dorsal view, 153, posterior view, 154, lateral view. 155, antenna. 156, pronotum and propleuron, frontal view.

FIGURES 157–161. Neuroterus niger Gillette, asexual generation, female. 157, mesosoma, lateral view. 158, mesosoma, dorsal view. 159, mesoscutellum, dorsal view. 160, metascutellum and propodeum, posterodorsal view. 161, metasoma, lateral view.

FIGURES 162–171. Neuroterus niger Gillette, sexual generation. 162–165, head, female: 162, frontal view, 163, dorsal view, 164, posterior view, 165, lateral view. 166, antenna, female. 167–170, head, male: 167, frontal view, 168, dorsal view, 169, posterior view, 170, lateral view. 171, antenna, male.

FIGURES 172–176. Neuroterus niger Gillette, sexual generation, female. 172, pronotum and propleuron, frontal view. 173, mesosoma, lateral view. 174, mesosoma, dorsal view. 175, mesoscutellum, dorsal view. 176, metascutellum and propodeum, posterodorsal view.

FIGURES 177–180. Neuroterus niger Gillette, sexual generation. 177, metasoma, lateral view, sexual female. 178–180, male: 178, metasoma, lateral view, 179–180, mesosoma: 179, dorsal view, 180, lateral view.

FIGURES 181–182. Neuroterus niger Gillette. 181, asexual gall. 182, sexual gall.