Cerroneuroterus apenninus ( Trotter, 1923 ) Cerasa & Sottile & Massa & Verde, 2021

Cerasa, Giuliano, Sottile, Salvatore, Massa, Bruno & Verde, Gabriella Lo, 2021, Rediscovery of Cerroneuroterus apenninus (Trotter, 1923) (Hymenoptera Cynipidae: Cynipini) a valid species from Italy with description and neotype designation, Zootaxa 4941 (3), pp. 399-414 : 403-411

Cerroneuroterus apenninus ( Trotter, 1923) comb. n.

Figs 6–41

Neuroterus sp. Trotter, 1903 (gall). Marcellia, 2(1): 16

Neuroterus apenninus Trotter, 1923 (gall). Marcellia, 20: 100

Study material. NEOTYPE ♀: ITALY: Emilia-Romagna, Bagno di Romagna, lago Pontini ex galls on Quercus cerris , 28.X.2017, 43°50’29.3”N 12°00’12.5”E, 770m, emerged 15.XII.2018 (sample N. 3427), S. Sottile leg. ( MSNG) . Other material: 2♀ with the same labels as the holotype, but “em. 28.XII.2018 ” (N. 3423) and (N. 3424), S. Sottile leg. ( GCPC) ; 1♀ with the same labels as the holotype “(N. 3425)” S. Sottile leg.; 3♀ with the same labels as the holotype, but “em. 15.XII.2019, 2♀ preserved in ethanol, (N. 3428) and 1♀ mounted on microscope slide in Hoyer’s liquid, (N. 3429) S. Sottile leg.; 1♀ with the same labels as the holotype, but “em. 05.01.2019 ”, (N. 3426) S. Sottile leg. ( SSPC) .

Additional material (Collected galls) ITALY: Emilia-Romagna, Bagno di Romagna, lago Pontini ex galls on Quercus cerris , 15.IX.1998 and 6.IX.2014, 43°50’29.3”N 12°00’12.5”E, 770m, G. Pezzi leg. ( GPPC and SSPC) ; ITALY: Campania, Parco Nazionale del Cilento, Sanza (Salerno), galls on Quercus cerris , 10.VIII.2015, 40°14’13.9”N 15°27’21.5”E, 870m, S. Sottile leg. ( SSPC) .

Diagnosis. Asexual females of C. apenninus comb. n. resemble the asexual females of C. gyulaigaraiae and C. lanuginosus from which it differs in having transscutal articulation partially lacking and reduced to a straight short median line in dorsal view ( Figs 21–23 , 31 ); mesoscutellum rounded, not elongated, as long as broad in dorsal view ( Fig. 22 ) while in C. gyulaigaraiae and C. lanuginosus transscutal articulation is totally lacking and mesoscutellum is elongated, longer than broad in dorsal view ( Figs 43, 45 ). In addition, C. apenninus comb. n. differs from C. gyulaigaraiae by having metascutellum broad, nearly 2.0 times as broad as high, equal or slightly higher than height of ventral impressed rim of metanotum in posterodorsal view ( Fig. 40 ); forewing 1.8 times as long as body; antenna with 12 flagellomeres nearly equal to body length while in C. gyulaigaraiae metascutellum is narrow, nearly as high as broad and 3.0–4.0 times as high as height of ventral impressed rim of metanotum ( Fig. 44 ); forewing is slightly longer than body; antenna with 13 flagellomeres slightly longer than half of body. Finally, adult females of the asexual generation of C. apenninus comb. n. are 1.6–1.8 mm; frons and vertex delicately alutaceous; propleuron alutaceous, smooth and glossy and latero-median and median area of pronotum alutaceous while in C. lanuginosus asexual generation adults are 2.6–3.0 mm in length; frons and vertex uniformly coriaceous; propleuron coriaceous with distinct irregular wrinkles, latero-median and median area of pronotum coriaceous.

Description. ASEXUAL FEMALE. Head dark brown, mandibles light brown, maxillary palps and labial palps yellowish; antennae brown; eyes black. Mesosoma brown, legs yellow-amber except for brown coxae, femura, Ts5 and tarsal claws. Metasoma dark brown. Wings hyaline, veins yellow-brown to brown.

Body length 1.6–1.8 mm.

Head nearly 1.2 times as broad as high in anterior view, 2.5 times as broad as long in dorsal view; frons and vertex delicately alutaceous, except for interocellar area delicately coriaceus, with very rare white setae and small impression below median ocellus, eyes long with very rare minute setae.

Lower face coriaceous with scattered piliferous point only on the central part, covered by sparse setae, with elevated median area; malar space delicately coriaceous, without malar sulcus and striae ( Fig. 15 ). Clypeus small, smooth, rounded, slightly sinuous, trapezoid ventral margin projecting over mandibles, marked by prominent epistomal sulcus, and with sparse setae or with piliferous point ( Fig 18 ); anterior tentorial pits and clypeo-pleurostomal line distinct, shallow, ventrally emarginated and deeply incised medially.

Gena alutaceous, broadened behind eye in front view, covered in sparse setae. Occiput alutaceous to delicately coriaceous with few white setae; postgena alutaceous to delicately coriaceous, with rare white setae; area around occipital foramen impressed, devoid of setae.

Postocciput around occipital foramen impressed; posterior tentorial pits large, ovate, deep; occipital foramen very slightly shorter than height of postgenal bridge, which is nearly 1.3 times shorter than length of oral foramen; gula smooth, glossy, narrowed in lower half; gular sulci weakly impressed, touching one another in the lower half of gula and curved outwards in the upper half ( Fig. 17 ); median sulcus of postgenal bridge with very delicate longitudinal striae. Malar space short, 0.2 times as long as height of compound eye. Transfacial distance 1.0–1.1 times as long as height of eye and 1.6 times as long as height of lower face (distance between antennal rim and tip of clypeus); diameter of torulus slightly greater than the distance between them; distance between torulus and inner margin of eye nearly 1.6 times diameter of torulus. Ocelli elliptical in shape, elevated over dorsal margin of head; POL 1.1 times as long as OOL; OOL 2.6 times as long as diameter of lateral ocellus and 1.4 times as long as LOL. Inner margins of eyes nearly parallel. Labial palpus 3–segmented, maxillar palpus 4–segmented. Antenna filiform, with 12 flagellomeres ( Fig. 16 ), nearly equal to body length, with dense long white setae on scape, pedicel and first eight flagellomeres gradually shorter in the last four segments; pedicel as long as broad, antenna increasing in thickness from F1 to F12, pedicel and scape 3.3 times broader than F1, 2.5 times than F2–F5, 2.0 times than F6–F8, 1.7 times than F9–F12; scape + pedicel nearly equal in length than F1, which is 1.2–1.3x longer than F2; F2–F4 nearly equal in length; F4 1.2x longer than F5; F5 slightly longer than F6 or F7; subsequent flagellomeres F8– F11 gradually decreasing in length; F12 1.7–1.8x longer than F11; placodeal sensilla present on F3–F12. Mesosoma very high, only 1.1–1.15 times as long as high. Pronotum glossy, with very few long white setae along antero-lateral edge and near pronotal spiracle, rare in other parts; anterior rim of pronotum narrow, emarginate; transverse pronotal sulcus present, deep with very few delicate striae near posteroventral corner of pronotum; posterolateral pronotal area, latero-median and median area of pronotum alutaceous without rugae ( Figs 25–26, 28 ). Propleuron alutaceous, smooth, glossy with sparse setae slightly concave in mediocentral part.

Mesoscutum smooth, glossy, with rare white setae along its lateral margin and rare adnotaular setae; 1.15 times as broad as long from above (width measured across base of tegulae); notauli complete, deeply impressed posteriorly and superficial in anterior half ( Figs 21, 23 ); median mesoscutal line absent; antero-admedian line not impressed, faintly visible in antero-dorsal view of mesosoma, parapsidal lines absent; parascutal carina narrow, anteriorly reaching notauli, mesoscutal suprahumeral sulcus not sculptured. Transscutal articulation reduced to a short and straight superficially median line; mesoscutum fused with the mesoscutellum with boundary between these structures that does not follow the transscutal articulation but slightly curved ( Figs 21–22 ).

Dorsomedian area of mesoscutellar-axillar complex (disc of mesoscutellum+axillar foveae), nearly as long as broad from dorsal view, rounded, not elongated, emarginated laterally and posteriorly, entirely and uniformly smooth and glossy, with sparse long white setae, slightly overhanging metanotum; the part which overhangs metanotum is areolate-rugose along lateral and posterior sides (visible in posteroventral view in Fig. 32 ).

Scutellar foveae in a form of narrow transverse groove anteriorly, more impressed than disk of mesoscutellum separated by a very weak central carina with smooth and glossy bottom with very few delicate wrinkles ( Fig. 22 ). Mesopleural triangle glossy with some delicate irregular short wrinkles and few white setae.

Mesopleuron and speculum entirely smooth, glossy and glabrous with very rare short white setae concentrated only close to the mesocoxal foramen. Pleurosternum smooth, glossy, with very delicatee short wrinkles near mesocoxal foramina; acetabular carina indistinct, epicnemia broad, finely alutaceous-imbricate ( Fig. 27 ). Metapleural sulcus distinct reaching mesopleuron in the upper 1/3 of its height; preaxilla smooth and glossy with few delicate rugae; dorsal axillar area smooth and glossy with sparse long setae, lateral axillar area smooth, glossy without setae; axillar carina broad, with longitudinal striae; axillula ovate smooth to delicate alutaceous and glossy without setae; subaxillular bar broad, smooth and glossy, at posterior end 1.5 times higher than height of metanotal trough; propodeal spiracle very slightly elevated, ovate.

Metascutellum trapezoidal, smooth and glossy, equal or slightly higher than height of ventral impressed rim of metanotum, which is smooth; metanotal trough smooth, glossy, without setae. Lateral propodeal carinae hardly traceable, indicated by some fragmented carinae curved outwards in the middle ( Figs 31–33 ), central propodeal area glabrous, smooth, glossy, without median propodeal vertical carina and with very few and delicate short wrinkles only near dorsal propodeal margin; lateral propodeal area smooth, glossy, with delicate irregular wrinkles and sparse white setae; nucha very short.

Forewing pubescent, hyaline, very weakly clouded around veins, 1.8 times as long as body, with distinct brown veins and very long marginal cilia; radial cell open, 6.2 times as long as broad; R1 and Rs reaching wing margin and extending along it; first abscissa of radius (2r) strongly curved, 2r–m straight; areoles distinct, triangular and large; 2r–m not extending along M vein; Rs + M distinct, reaching basal vein in the lower half ( Fig. 29 ). Hindwing, pubescent, hyaline, with very long marginal cilia and narrow infuscate stripe on the anterior margin, starting from hamuli and extending along the margin for around 1/2 of its length ( Fig. 30 ).

All tarsal segments longer than broad, Ts1 the longest one; hind tarsal claws simple, without basal lobe; fore tarsomere I (Ts1) to V (Ts5) length ratio as 1.0:0.4:0.3:0.2:0.4; tibial spur long, curved inward, bifid at apex, nearly 0.35 times as long as basitarsus of foreleg ( Fig. 37 ).

Metasoma nearly 1.3 times shorter than mesosoma and nearly 1.6 times shorter than head+mesosoma. Metasoma strongly compressed laterally, 0.7 times as long as high in lateral view, smooth, glossy, with rare and scattered white setae in T2 antero-laterally ( Fig. 34 ), all metasomal tergites and hypopygium without micropunctures; T2 occupying nearly 1/2 length of metasoma; prominent part of ventral spine of hypopygium extremely short, as long as broad ventrally (in some specimens very short, 2.0 times longer than broad in ventral view), with long white setae, extending beyond apex of spine but never forming a tuft ( Figs 35–36 ).

Gall ( Figs 6 , 8–14 , 54–60 ). [Original description by Trotter 1903, translated from Italian] “… This is to be considered among the most curious leaf galls of this oak (…he was referring to Quercus cerris ). On the lower page of the leaf at first, you can see only a very dense felt or fluff more or less extensive, consisting of hairs of a very characteristic color, red-wine, with some fawn shades. Looking more closely, or rather to rummage through these hairs, you can see numerous, small, yellowish galls, very close to each other, ovoids transversely, at most 1 mm long, with very thin and fragile walls which are covered by the fluff mentioned above. These galls adhere to the foil, and indeed affect its entire thickness, appearing even slightly from the side of the upper page in the manner of minute brown callosity, a little wrinkled, with a diameter of just over 0.5 mm. These galls at their base, when detached, are attenuated in a very short peduncle. The hairs that cover the galls are cylindrical, twisted, very thin (20–25\x thick) attenuated at the apex, multicellular, sometimes a little strangled at the septa, or even made up of cell segments of unequal thickness (fig. 7). The hairs are about 3–5 mm long, therefore much more than the gall. Even if these galls had already been collected for several years, it was not possible for me to observe the producer, which I certainly ascribe to the cynipids and probably, for reasons of analogy, to the gen. Neuroterus . A Chiusdino (Tuscany) September 26, 1895, G. Cuboni; Leonessa, September 1895 C. Rodriguez”.

In addition, we have counted from 80 to 200 small galls coalescent in the “islands” of fluff in a single leaf, most of which generally without larvae; the wall of the larval chamber is thick at the beginning of development ( Fig. 13 ) and becomes thinner to maturity ( Fig. 14 ) as the nutritive tissue is consumed. The long cylindrical multicellular hairs with a diameter greater at the septa ( Figs 59, 60 ) cover the single galls and keep them together piled up on the leaf lamina. At the same time, they protect the galls from the attack of inquilines and parasitoids, as done by accessory and defensive structures present in the galls of other cynipids.

Similar galls. Asexual generation galls of Cerroneuroterus apenninus comb. n. belong to the group of “cotton or woolly gall” (e.g. Andricus quercusramuli (Linnaeus, 1761) sexual generation and also Cynips korsakovi Belizin, 1961 asexual generation) whose larval chambers are coalescent in the “islands” of fluff and completely hidden among the hair.

The only similar galls of C. apenninus comb. n. are the galls of Cynips korsakovi Belizin, 1961 , but differ in the spherical shape of the larval chambers, which are instead pyriform in C. korsakovi ; in addition, the galls of C. korsakovi develop on Quercus section oaks.

Galls of similar species. The galls of the similar species C. lanuginosus and C. gyulaigaraiae belong to the group of “spangle gall” (e.g. Neuroterus numismalis ag. and C. gyulaigaraiae ) due to their flattened shape and to the presence of a navel in the center of the gall, and differ from C. apenninus comb. n. galls by the characters listed in Table 2 .

Biology. Only the asexual generation of C. apenninus comb. n. is known. The galls begin to develop on Q. cerris probably in early summer and during the first half of October, after completing their development, fall slightly before leaf fall so ensuring a covering of leaves and a more suitable microclimate for diapausing insects. Our data show that adults emerge one year after the full development of their galls and it could be hypothesised that a sexual generation can develop on oaks of the Quercus sect. Cerris, probably on buds or twigs.

Distribution. Currently known only from Emilia Romagna, Tuscany, Latium and Campania regions in Italy. The species probably occurs throughout the Apennine mountains.

Figures

FIGURES 1–7. 1–2, Envelopes containing galls reported as Neuroterus apenninus by Trotter, original preserved in the ‘Cecidotheca italica’ by Trotter & Cecconi at the Botanical Garden of Padua (by courtesy of Padua University); 3, original drawing of section of the same gall and the multicellular cylindrical hairs that cover the galls indicated by the arrows (from Trotter 1903); 4–5, details of plastic jars in which the galls were kept; 6, oval cells of galls of Cerroneuroterus apenninus comb. n., the lateral view showing the arrangement of long hairs; 7, asexual female of the same species, habitus in lateral view.

FIGURES 8–14. Galls of Cerroneuroterus apenninus comb. n.: 8, general appearance of gall; 9, magnification of the cell group; 10, marks on the upper page of the leaf at the galls; 11, ventral view of the gall howing the peduncle; 12, single cell of the gall in lateral view; 13–14, dissected gall, showing the larval chamber: 13, during early development and 14, at maturity.

FIGURES 15–23. Cerroneuroterus apenninus comb. n.: 15, head, (front view); 16, antenna; 17, head, (posterior view); 18, head, (ventral view); 19, head (lateral view); 20, head (dorsal view); 21, mesosoma (dorsal view); 22, mesoscutellum (dorsal view); 23, mesosoma (latero-dorsal view).

FIGURES 24–30. Cerroneuroterus apenninus comb. n.: 24, mesosoma (lateral view); 25, pronotum, (anterodorsal view); 26, pronotum, (latero-ventral view); 27, mesosoma (ventral view); 28, mesosoma (latero-ventral view); 29, forewing; 30, hindwing.

FIGURES 31–39. Cerroneuroterus apenninus comb. n.: 31–33, metascutellum and propodeum, posterodorsal and posteroventral view; 34, metasoma (lateral view); 35, ventral spine of hypopygium (lateral view); 36, ventral spine of hypopygium, ventral view; 37, foreleg, female, the arrow shows the magnification of simple tarsal claws; 38, mid tarsus and mid tibial spur, female; 39, hind tarsus and hind tibial spur, female.

FIGURES 40–45. 40–41, Cerroneuroterus apenninus comb. n. asexual female: 40, metascutellum and propodeum, posterodorsal view; 41, mesoscutellum, dorsal view; 42–43, C. lanuginosus asexual female (illustration by Melika, 2006b): 42, metascutellum and propodeum, posterodorsal view; 43, mesoscutellum, dorsal view; 44–45, C. gyulaigaraiae asexual female (illustration by Melika, 2006a): 44, metascutellum and propodeum, posterodorsal view; 45, mesoscutellum, dorsal view.

FIGURES 46–60. Comparison between asexual generarion galls of Cerroneuroterus lanuginosus and C. apenninus comb. n. 46–53, C. lanuginosus galls: 46, general appearance of gall on the underside of the leaf and 47, upper side of the same leaf; 48–50, galls in lateral view; 51–52, dissected gall, showing the spongy tissue that surrounding the hard-walled central chamber; 53, histological preparation showing unicellular cylindrical hairs; 54–60, C. apenninus comb. n. galls: 54, 57, general appearance of gall on the underside of the leaf and 55, upper side of the same leaf with minute brown callosity; 56, gall in lateral view; 58, dissected gall, showing the thin suberous wall of the larval chamber; 59–60, histological preparation showing multicellular cylindrical hairs, the arrow shows the intercellular septa.

Tables

TABLE 2. Morphological differences between galls of the congeneric similar species Cerroneuroterus lanuginosus, C. gyulaigaraiae, C. apenninus comb. n.

			Cerroneuroterus lanuginosus	Cerroneuroterus gyulaigaraiae	Cerroneuroterus apenninus
Type of gall			“spangle gall” (on the underside of the leaf) (Figs 46, 48)	“spangle gall” (on the underside of the leaf)	“cotton or woolly gall” (on the underside of the leaf) (Figs 54, 57)
Shape			The gall is flat (Figs 48–50)	The gall is flat	The gall is rounded or drop- shaped (Figs 56, 58)
Gall size			4-5 mm in diameter, 3-4 mm high	2–4 mm in diameter, 1.5–2.0 mm high	…at most 1-1.5 mm long
Number of galls on the leaf			usually found in groups (up to 50)	usually found in small groups (up to 5–6)	usually found in big groups (80 to 200 small galls)
Upper side of the leaf lamina			The gall does not erupt through the upper surface of the leaf, but forms a small pale mark on the upper surface indicating a gall beneath ( Melika, 2006b). The numerous galls collected on Q. suber and Q. cerris in our collections do not have any marks in correspondence on the upper surface of the leaves (Fig. 47).	The gall does not erupt through the upper surface of the leaf, but forms a small pale mark on the upper surface indicating a gall beneath.	Appearing even slightly from the side of the upper page in the manner of minute brown callosity, a little wrinkled, with a diameter of just over 0.5 mm (Fig. 55).
Tissues surrounding			Thick and spongy-like (Figs	Thick and spongy-like.	Very thin and not-spongy
the larval chambers mature galls		in	51–52).		(Fig. 58).
Wall of the chambers	larval		In the centre of the spongy tissue there is a hard-walled central chamber, slightly flattened; small spaces surround the chamber laterally (Figs 51– 52).	In the centre of the spongy tissue there is a hard-walled central larval chamber, which is not surrounded by air chambers, parenchima around the central larval chamber thick and hard.	In mature galls the wall of the larval chambers is very thin with a suberous fragile consistency (Fig. 58).
Length of hair			Length of hair less than 1.5 times the height of gall (Figs 48, 50–51).	Short pale silk.	Length of hair more than two times the height of gall (Fig. 56).
Histological feature of hairs			Unicellular cylindrical hairs (Fig. 53)	Unknown	Cylindrical multicellular with a larger diameter near the septa and constituted by cell segments of unequal thickness (Figs 59, 60).
References			Melika, 2006b	Melika, 2006a	Cerasa et al. (present paper)