Andricus pseudomultiplicatus Sottile, Nicholls & Cerasa, 2025

Andricus pseudomultiplicatus Sottile, Nicholls & Cerasa , sp. nov.

Figs 7–9 View FIGURES 1–9 ; 10–15 View FIGURES 10–15 ; 44–76 View FIGURES 44–54 View FIGURES 55–65 View FIGURES 66–76

Type material. HOLOTYPE 1♂ & 1♀ (deposited in MSNG), card-mounted. ITALY: Emilia-Romagna, Vernasca ( PC), ex galls on Quercus cerris , 20.IV.2024, 44.790164, 9.786095, 440 m, emerged 8.V.2024 (samples N.5280, N.5300), S. Sottile leg. “ Holotype Andricus pseudomultiplicatus sp. n. Sottile, Nicholls et Cerasa” (red). GoogleMaps

PARATYPES with white label “Paratype Andricus pseudomultiplicatus sp. n. Sottile, Nicholls et Cerasa”: 58♂: ITALY: Emilia-Romagna, Vernasca (PC), ex galls on Quercus cerris , 20.IV.2024, 44.790164, 9.786095, 440 m, emerged 3–12.V.2024, (samples N. 5281–N.5298 ) ( MSNG, MCLSS, GCPC, SSPC) GoogleMaps ; 27♀: with same label but emerged 3–14.V.2024 (samples N.5299–N.5307 ) ( MSNG, MCLSS, GCPC, SSPC) .

Material used for molecular analysis. 1♀: ITALY: Emilia-Romagna, Alseno ( PC) , ex galls on Quercus cerris , 6.V.2018, 44.852526, 9.952569, 180 m, emerged 10.V.2018 (sample N.3503-B); 1♂: HUNGARY: Matrafured, ex galls collected 21.V.2001 on Q. cerris , emerged 28.V.2001, labels HP14477 and Andmul 20 ( GSPC) ; 1♀: HUNGARY: Matrafured, ex galls collected 11.V.2001 on Q. cerris , emerged 5.VI.2001, labels HP12932 and Andmul 38 ( GSPC) ; 2♂: ITALY, ex galls collected on Q. cerris , labels Andmul 70 and Andmul 71 ( GSPC) . All material used for this molecular work was also confirmed as A. pseudomultiplicatus sp. nov. using adult morphology.

Additional material examined. 14♀: ITALY: Emilia-Romagna, Alseno ( PC) , ex galls on Quercus cerris , 6.V.2018, 44.852526, 9.952569, 180 m, emerged 8–10.V.2018 (samples N.3499–N.3504), S. Sottile leg. ( MSNG, MCLSS, GCPC, SSPC) GoogleMaps ; 2♀: with same label but mounted in Hoyer’s medium on microscope slides (V.360, V.361) ( SSPC) ; 4♀: with same label but collected 15.V.2021, emerged 20.V.2021 (samples N.4274, N.4275) ( SSPC) ; 18♀: ITALY: Toscana, Empoli ( FI) , ex galls on Quercus cerris , 2.V.2023, 43.701439, 10.937414, 120 m, emerged 3–8.V.2023 (samples N.4849–N.4854), Fabrizio Mujica leg. ( SSPC, MSNG, MCLSS) GoogleMaps ; 3♂ & 10♀: ITALY: Emilia-Romagna, Vernasca ( PC) , ex galls on Quercus cerris , 20.IV.2024, 44.790164, 9.786095, 440 m, emerged 3–12.V.2024 (preserved in 95 % ethanol), S. Sottile leg. ( SSPC) GoogleMaps .

Diagnosis. A. pseudomultiplicatus sp. nov. has such distinctive features that it could never be confused with any other sexual Andricus currently described from the Western Palaearctic. Among those sexual Andricus , the only comparable species are A. crispator and A. istvani ; all three species share the distinguishing character state of an absence of setae on the forewing margins of females ( Tavakoli et al. 2008; Nieves-Aldrey, 2009). The new species and A. crispator are distinguishable by the following features. In females of A. pseudomultiplicatus sp. nov., body length 1.25–1.35 mm (1.5–1.6 mm in A. crispator ); mesoscutum 1.1 times wider than long in dorsal view and 1.5–1.7 times as long as the mesoscutellum (1.3 times wider than long in dorsal view and 1.2–1.3 times as long as the mesoscutellum in A. crispator ); mesoscutellum not rounded posteriorly and ending in a point, strongly rugose especially near the margins and posteriorly (posteriorly rounded or truncated but not pointed, moderately rugose across the entire surface in A. crispator ); prominent part of ventral spine of hypopygium less slender, 3.5–4.5 times as long as broad in ventral view (slender, 5.3–5.7 times as long as broad in ventral view in A. crispator ); in males of A. pseudomultiplicatus sp. nov. POL 1.7–1.8 times as long as OOL (1.5–1.6 times in A. crispator ); OOL 2.1–2.2 times as long as diameter of lateral ocellus and 1.1 times as long as LOL (1.8–2.0 times as long as diameter of lateral ocellus in A. crispator ); distance between torulus and inner margin of eye nearly 3.0 times the distance between toruli (nearly 1.5 times the distance between toruli in A. crispator ); mesoscutum shallowly reticulate in the internotali area, more weakly on the remaining parts, 1.4–1.5 times as long as the mesoscutellum (strongly reticulate across the entire surface, 1.6–1.7 times as long as the mesoscutellum in A. crispator ); internotauli width at posterior margin of mesoscutum is 1.5–1.6 times the width of one notaulus at the same point (1.7–1.8 times the width of one notaulus at the same point in A. crispator ).

Description. SEXUAL FEMALE. Body with sparse white setae, predominantly amber-colored; antenna slightly lighter than body, excluding the distal half which is darkened; eyes black; legs yellow-amber except for light brown Ts5 and tarsal claws. Mesosoma and metasoma amber to brown, dorsally much darker, with the metasoma relatively darker. Body length 1.1–1.35 mm (N = 27).

Head ( Figs 44–48 View FIGURES 44–54 ) with very sparse white setae, nearly 1.2–1.3 times as broad as high in frontal view, 2.0–2.1 times as broad as long in dorsal view. Lower face coriaceous to shallowly reticulate, with striae radiating from clypeo-pleurostomal line but present only near the ventral margin of the head, not reaching eye and not present medially on the lower face, malar sulcus absent ( Figs 16, 19 View FIGURES 16–24 ). Clypeus ( Figs 44, 47 View FIGURES 44–54 ) smooth, subtrapezoidal, ventral margin projecting over mandibles with distinct anterior tentorial pits, epistomal sulcus and clypeo-pleurostomal line only slightly impressed. Malar space 0.3–0.4 times as long as height of compound eye. Transfacial distance 1.2–1.3 times as long as height of eye and 1.7–1.8 times as long as height of lower face (distance between antennal rim and tip of clypeus); diameter of torulus about 1.6–1.8 times as long as distance between toruli; distance between torulus and inner margin of eye 1.5 times diameter of torulus. Inner margins of eyes distinctly convergent ventrally. Gena delicately reticulate ( Figs 46–47 View FIGURES 44–54 ), only very slightly broadened behind eye in front view, with only rare setae. Frons, vertex and interocellar area uniformly reticulate, with irregular dark spot in the ocellar area in some specimens ( Fig. 48 View FIGURES 44–54 ). Ocelli oval in shape, elevated over dorsal margin of head; POL 1.2–1.3 times as long as OOL; OOL 3.5–4.0 times as long as diameter of lateral ocellus and 1.6–1.7 times as long as LOL. Occiput coriaceous to shallowly reticulate with rare white setae; postgena coriaceous to reticulate, with very sparse white setae; area around occipital foramen impressed, without or with only rare setae. Postocciput around occipital foramen impressed; posterior tentorial pits distinct, elongate, deep; occipital foramen slightly shorter than height of postgenal bridge, which is nearly 1.4 times shorter than length of oral foramen; gula narrowed in lower half with very few and delicate longitudinal striae in lower half; gular sulci very weakly impressed, curved outwards in the upper half ( Fig. 45 View FIGURES 44–54 ). Labial palpus 3–segmented, maxillar palpus 4-segmented.

Antenna ( Figs 53, 54 View FIGURES 44–54 ) with 10 flagellomeres (but the last sometimes with an indistinct, incomplete suture, so appears as 11 flagellomeres), 1.3–1.4 times as long as head+mesosoma and 0.8 times shorter than body length, with sparse white setae on scape, pedicel and first four flagellomeres, setae gradually denser and shorter on the last seven segments; placodeal sensilla present on F4–F10; pedicel about 1.6 times as long as broad, scape + pedicel 1.8–2.0 times longer than F1, which is 1.3–1.4 times longer than F2, F2–F6 nearly equal in length, subsequent flagellomeres F7–F9 slightly shorter and gradually decreasing in length, F10, 2.0–2.1 times longer than F9; all flagellomeres longer than wide.

Mesosoma 1.2–1.3 times as long as high in lateral view ( Fig. 50 View FIGURES 44–54 ). Pronotum ( Figs 50 View FIGURES 44–54 , 55 View FIGURES 55–65 ) reticulate with some wrinkles in lateral and posterolateral pronotal area and near posteroventral corner, shiny, with a few white setae concentrated near anterior rim and posteroventral corner of pronotum; anterior rim of pronotum narrow, emarginate; transverse pronotal sulcus present, shallow, striate. Dorsal part of pronotal plate distinctly offset, with anterolateral corners, ventral and lateral margins marked; posterolateral tooth-like section of anterior part of pronotal plate present ( Fig. 55 View FIGURES 55–65 ).

Propleuron ( Fig. 59 View FIGURES 55–65 ) weakly reticulate, shiny with rare short setae. Mesoscutum reticulate in between the notali, more weakly reticulate on the remaining parts ( Fig. 49 View FIGURES 44–54 ), shiny, with rare white setae along the lateral margin and rare adnotaular setae; 1.15–1.25 times as broad as long from above (width measured across base of tegulae); notauli complete, broad, deep and well-impressed along total length, with wide smooth, shining bottom, converging and almost confluent at posterior end near to the posterior margin of mesoscutum, where internotauli width is 1.3 times the width of one notaulus at the same point; median mesoscutal line visible, short, in the form of a triangle, extending less than 1/5 of the total length of the mesoscutum ( Fig. 51 View FIGURES 44–54 ); antero-admedian line absent, parapsidal lines absent but indicated by narrow stripes of smooth sculpture; parascutal carina narrow, anteriorly reaching notauli, mesoscutal suprahumeral sulcus strongly reticulate. Transscutal articulation deep, distinct. Dorsomedian area of mesoscutellaraxillar complex (disc of mesoscutellum+axillar foveae; Fig. 49 View FIGURES 44–54 ) 1.5–1.7 times shorter than mesoscutum, nearly as long as broad from dorsal view, pentagonal, strongly rugose especially near the margins and posteriorly, very slightly emarginated laterally but not posteriorly, with rare long white setae, clearly overhanging metanotum in lateral view ( Fig. 50 View FIGURES 44–54 ), clearly visible also in ventral view ( Fig. 56 View FIGURES 55–65 ). Scutellar foveae ( Fig. 49 View FIGURES 44–54 ) ellipsoidal, 1.7–1.8 times broader than high, deep with smooth and shiny bottom weakly delimited posteriorly and separated by distinct, central carina.

Mesopleural triangle smooth with some delicate striae and a few white setae. Mesopleuron and speculum ( Figs 14 View FIGURES 10–15 , 50, 52 View FIGURES 44–54 ) shiny, uniformly transversely striate; essentially glabrous except for rare short white setae on anteroventral part and (more densely) on posteroventral part. Pleurosternum smooth, shiny, with delicate wrinkles and white setae between mesocoxal foramina and near mesodiscrimen; metasubpleuron smooth, shiny, with delicate wrinkles and dense long white setae; acetabular carina ( Fig. 59 View FIGURES 55–65 ) well developed, epicnemia broad, from alutaceous to finely coriaceous. Metapleural sulcus distinct, reaching mesopleuron in the upper 1/3 of its height ( Fig. 50 View FIGURES 44–54 ); areas delimited by the inferior parts of metapleural sulcus coriaceous with dense white setae and some delicate wrinkles; preaxilla smooth and shiny with a few delicate rugae; dorsal axillar area delicately reticulate with rare long setae, lateral axillar area smooth and shiny with some delicate wrinkles; axillar carina distinct, broad, with longitudinal curved distinct striae, without setae; axillula subtriangular, smooth, glossy, with dense white setae; subaxillular bar narrow, smooth and glossy, at most posterior end nearly equal to or slightly higher than height of metanotal trough ( Fig. 50 View FIGURES 44–54 ); propodeal spiracle very slightly elevated, ovate, carina extending from spiracle distinctly raised; pit above spiracle deep, smooth, glossy; area between metapleural sulcus and spiracle glossy, with some punctures and long setae.

Metascutellum ( Fig. 60 View FIGURES 55–65 ) trapezoidal, smooth and shiny, metascutellum narrow, nearly 3.5 times as broad as high and 0.75 times shorter than height of ventral impressed rim of metanotum in posterodorsal view which is smooth; metanotal trough narrow, smooth, and glossy, with rare white setae. Lateral propodeal carinae distinct and percurrent, slightly curved outwards in the middle ( Fig. 60 View FIGURES 55–65 ), strong and uniformly thick, carinae end dorsally in a thick protruding small process; central propodeal area glabrous, smooth, shiny, without median propodeal vertical carina and without setae; central propodeal area short, more than 2.1 times broader than long, with its height slightly shorter than height of metascutellum+height of ventral impressed rim of metanotum; lateral propodeal area alutaceous with some very delicate rugae and with relatively dense white setae; nucha short, with irregular wrinkles dorsally and laterally ( Fig. 60 View FIGURES 55–65 ).

Forewing ( Fig. 57 View FIGURES 55–65 ) 2.4 times as long as wide, 1.5–1.6 times as long as body, hyaline, with micro-pubescent surface, with extremely short marginal setae; very weakly clouded around veins, with distinct light brown veins; radial cell open, 3.6–3.8 times as long as broad; R1 short, 0.5–0.6 times shorter than first abscissa of radius (2r), not reaching wing margin, Rs nearly reaching wing margin and extending along it; 2r slightly curved; 2r–m straight; areolet distinct, triangular, in some cases very small (within the same specimen, often one of the two forewings possesses a smaller areolet); 2r–m not extending along M vein; Rs+M weakly marked, extending to 2/3 distance between areolet and basal vein and projecting slightly below midpoint of basal vein. Hindwing ( Fig. 58 View FIGURES 55–65 ), 4.0– 5.0 times as long as wide, hyaline, with micro-pubescent surface and long marginal setae (marginal setae length/ hindwing width=0.15–0.20), R1 vein very faintly visible.

All tarsal segments longer than broad, except Ts5 as long as broad, Ts1 the longest one; tarsal claws with basal lobe; fore Ts1 to Ts5 length ratios are 1.0:0.4:0.35:0.3:0.7; tibial spur slightly curved inward, bifid at apex, nearly 0.5 times as long as basitarsus of foreleg ( Fig. 62 View FIGURES 55–65 ).

Metasoma 0.8–0.9 times as long as head+mesosoma and slightly higher than long in lateral view, smooth, shiny, with sparse white setae on T2 antero-laterally ( Fig. 61 View FIGURES 55–65 ); metasomal tergum 2 without micropunctures, subsequent terga with very indistinct micropunctures; prominent part of ventral spine of hypopygium 3.5–4.5 times as long as broad in ventral view, with rare, white setae; setae have a length about 1.2 times the median diameter of the hypopygium in lateral view, are straight, do not extend beyond apex of spine and never form a tuft ( Figs 61, 65 View FIGURES 55–65 ).

MALE. Body length 1.05–1.35 mm (N = 58). Similar to female in colour, except for mesosoma which is darker dorsally and antennae slightly lighter than body even at the distal end.

Compound eyes and ocelli bigger than in female ( Figs 66–68 View FIGURES 66–76 ); POL 1.7–1.8 times as long as OOL; OOL 1.8–1.9 times as long as diameter of lateral ocellus. Malar space shorter (0.2–0.3 times as long as eye height). Transfacial distance equal to or slightly longer than height of eye and 1.5–1.6 times as long as height of lower face; distance between torulus and inner margin of eye nearly equal to diameter of torulus and nearly 3.0 times the distance between toruli ( Fig. 66 View FIGURES 66–76 ).

Antenna ( Figs 69–70 View FIGURES 66–76 ) with 12 flagellomeres; with short dense white setae uniformly distributed on all segments; placodeal sensilla present on all flagellomeres. Pedicel about 1.3 times as long as broad, all flagellomeres nearly of the same width; F1 modified, slightly excavated in basal half and swollen apically ( Fig. 70 View FIGURES 66–76 ); scape+pedicel 1.5–1.6 times longer than F1, which is nearly equal to or slightly longer than F2, F2 1.1x longer than F3–F7 and 1.2–1.3x longer than F8–F12. Internotauli width at posterior margin of mesoscutum is 1.5–1.6 times the width of one notaulus at the same point. Mesoscutum weakly reticulate. Lateral propodeal carinae distinct and percurrent, very slightly curved outwards in the middle ( Fig. 73 View FIGURES 66–76 ); central propodeal area 1.2–1.3 times broader than long, with its height equal to twice the height of metascutellum+height of ventral impressed rim of metanotum. Forewing ( Fig. 75 View FIGURES 66–76 ) 2.4– 2.5 times as long as wide, hyaline, with a normally pubescent surface and distinct marginal setae (marginal setae length/forewing width=0.06); 1.4–1.5 times as long as body; radial cell open, 3.1–3.2 times as long as broad; R1 short, 0.7–0.8 times shorter than first abscissa of radius (2r), nearly reaching wing margin, Rs nearly reaching wing margin and extending along it; 2r slightly curved; 2r–m nearly straight; areolet distinct, triangular, in some cases very small (often within the same specimen, one of the two wings possesses a smaller areolet); 2r–m not or very slightly extending along M vein; Rs+M weakly marked, extending to 2/3 distance between areolet and basal vein and projecting slightly below midpoint of basal vein. Hindwing ( Fig. 76 View FIGURES 66–76 ), 4.0–4.5 times as long as wide, hyaline, with a normally pubescent surface and long marginal setae (marginal setae length/forewing width=0.15–0.20); R1 vein visible in the form of an infuscate stripe on the anterior margin.

Galls and Biology ( Figs 7–9 View FIGURES 1–9 , 10–13 View FIGURES 10–15 ). Only the sexual generation is known, and induces multilocular galls on Quercus cerris L. (section Cerris ). Galls develop on the leaves, petiole, and along the main veins. Externally, they appear as irregular swellings, asymmetrical towards the underside of the leaf, primarily affecting the veins but causing deformation of the leaf blade, which becomes folded upon itself in a disordered manner. Galls are light yellowish-green, and in the initial development phase they appear translucent-glassy and succulent. They are covered with normal trichomes, continuous with those of the host leaf. Larval chambers are present in the invagination induced on the leaf blade, are ovoid-ellipsoid in shape, approximately 1.7–2.1 mm in height, and attached at one end to the swollen and deformed vein, which serves as the germinal substrate. They are formed of a coriaceous wall, covered with whitish, unicellular hairs up to 0.3 mm long, which are either straight or sinuous and slightly denser at the chamber’s apical end. Each leaf gall contains between one and ten larval chambers, typically three or four; a single insect develops in each larval chamber. The larva develops rapidly, has a short pupal stage, and the insect emerges by creating a large hole at the apical end of the chamber.

The leaves on which the galls develop may exhibit reduced growth and tend to dry out and detach prematurely from the host plant. As the galls mature, dehydration causes a reduction in volume in the swollen and succulent region, resulting in the larval chambers becoming firmly adhered to the upper surface of the leaf blade. These sexual generation galls begin to develop in April and the adults emerge in May.

The biology of other closely-related congeneric species suggests that this species should have the heteroecic host-alternating life cycle typical of this group of Andricus species, and that galls of its asexual generation should be found on sympatric oaks of the section Quercus (e.g., Q. petraea , Q. pubescens , Q. robur ).

Molecular results. Sequences obtained from individuals that had been confirmed morphologically as A. pseudomultiplicatus sp. nov. grouped together with an ultra-fast bootstrap value of 100% ( Fig. 42 View FIGURE 42 ). ITS2 sequences from this species also clustered together within minimal variation amongst them compared to between-species differences ( Fig. 43 View FIGURE 43 ). This grouping also included the specimen sequenced by Stone et al. (2009) that had been mis-identified as the species A. multiplicatus (terminal labelled as ‘pseudomultiplicatus _5’ in Fig. 42 View FIGURE 42 ; GenBank accessions DQ217996 View Materials & DQ217970 View Materials which were used in this analysis, as well as accession DQ201499 View Materials ), thus explaining the generation-matching discrepancy between the experimental rearings of Sottile et al. 2023 that linked A. multiplicatus with A. truncicolus and Stone et al.’s (2009) discordant phylogenetic result for these taxa. Some phylogeographic structure was also apparent within this species, with reciprocally monophyletic groupings of Italian versus Hungarian specimens ( Fig. 42 View FIGURE 42 ).

The new species A. pseudomultiplicatus formed part of a well-supported clade (ultra-fast bootstrap value of 97%) that also included A. istvani and A. crispator , the other two Western Palaearctic Andricus species that share the distinctive character state of a lack of marginal setae on the sexual female’s forewing ( Fig. 42 View FIGURE 42 ). This clade falls towards the base of the large group of Western Palaearctic host-alternating Andricus species, and its constituent species are only known from their sexual generations, making integral, multilocular or aggregated, leaf galls on section Cerris oaks .

Etymology. Pseudo, derived from Greek, is the first element of compound words in which it has the meaning of “false”. The galls of the new species can be confused with Andricus multiplicatus (here determined to be a junior synonym of A. truncicolus ), so we have therefore named this species with the meaning of “false multiplicatus”.

Distribution. Currently known from Italy in the Emilia-Romagna and Tuscany regions and from multiple locations within Hungary. However, the similarity of this species’ galls to the sexual galls of other species such as A. truncicolus and A. conificus means that we may not currently have a clear idea of the full geographical range of any of these species.