Necremnus tutae, Gebiola, Marco, Bernardo, Umberto, Ribes, Antoni & Gibson, Gary A. P., 2015

Gebiola, Marco, Bernardo, Umberto, Ribes, Antoni & Gibson, Gary A. P., 2015, An integrative study of Necremnus Thomson (Hymenoptera: Eulophidae) associated with invasive pests in Europe and North America: taxonomic and ecological implications, Zoological Journal of the Linnean Society 173 (2), pp. 352-423 : 382-385

NECREMNUS TUTAE RIBES & BERNARDO SP. NOV.

( FIGS 48–56 )

Etymology

Named after the genus of its host, Tuta absoluta (Meyrick, 1917) (Lep., Gelechiidae ).

Type material

Holotype ♀: SPAIN: Cabrils, Barcelona, ex. Tuta absoluta on Solanum lycopersicum , 17.v.2011, IRTA culture. Allotype ♂: same data as holotype. Paratypes (28♀ 18♂): ITALY: 10♀ 3♂, Liguria, ex. Tuta absoluta on Solanum lycopersicum, 2012 , Bioplanet culture. SPAIN: 5♀ 5♂, same data as holotype; 13♀ 10♂, same data as holotype, except dates 29.iii−15.xii.2011. The holotype, allotype, and some paratypes are deposited in CNC, and some paratypes in BMNH and the A. Ribes and U. Bernardo’s collection.

Additional material (36♀ 31♂): ALGERIA: 1♀, Mostaganem, ex. Tuta absoluta on Solanum lycopersicum , 24.iv.2011. FRANCE: 4♀ 1♂, Berrel’Etang, Rhone, Provence, ex. Tuta absoluta on Solanum lycopersicum , 23.vi.2010 − 20.vi.2011; 2♀, Antibes, Alpes Maritimes, ex. Tuta absoluta on Solanum lycopersicum , 23.vi.2011. MOROCCO: 6♀ 6♂, Souss-Massa Valley, ex. Tuta absoluta on Solanum lycopersicum , v.2010, leg. S. Amazouz. ITALY: 2♀ 3♂, Liguria, Bioplanet culture, ex. Tuta absoluta on Solanum lycopersicum, 2011 –2012; 1♀, Pagani (SA), Campania, ex. Tuta absoluta on Solanum lycopersicum , 20.x.2010, leg. U. Bernardo; 2♀, Poggiomarino (NA), Campania, ex. Tuta absoluta on Solanum lycopersicum , 10–12.x.2010, leg. U. Bernardo; 1♂, Marigliano (NA), Campania, ex. Tuta absoluta on Solanum lycopersicum , 12.x.2010, leg. U. Bernardo; 1♂, Capaccio (SA), Campania, ex. Tuta absoluta on Solanum lycopersicum , 23.x.2011, leg. U. Bernardo; 3♀ 2♂, Pula (CA), Sardegna, ex. Tuta absoluta on Solanum lycopersicum , 8.viii.2009 − 23.vi.2010, leg. F. Sanna; 3♀ 1♂, Assemini, Sardegna, ex. Tuta absoluta on Solanum lycopersicum , vii.2009 [BMNH]. LIBYA: 3♀, W. of Tripoli, Anjilaa, ex Tuta absoluta on Solanum lycopersicum , 15.vi.2010 [BMNH]. SPAIN: 1♀ 3♂, Cabrils, Barcelona, ex. Tuta absoluta on Solanum lycopersicum , 4.x.2010, leg. R. Gabarra, IRTA; 4♀ 5♂, Blanes, Barcelona, ex. Tuta absoluta on Solanum lycopersicum , 4.x.2010, leg. IRTA; 6♀ 6♂, Cabrera de Mar, Barcelona, ex. Tuta absoluta on Solanum lycopersicum , 4.x.2010, leg. IRTA; 2♀, Mareny, Valencia, ex. Tuta absoluta on Solanum lycopersicum , vi.2008; 9♀ 9♂, La Mojonera, Almeria, ex. Tuta absoluta on Solanum lycopersicum , vi.2011. TUNISIA: 1♀, Kairouan, ex. Tuta absoluta on Solanum lycopersicum , v.2012, leg. K. Abbes.

Diagnosis

Female

Gaster ( Figs 48, 49 ) ovate, 1.9–2.4 × as long as broad, 1.2–1.5 × as long as mesosoma, and 0.95–1.2 × as long as head plus mesosoma; syntergum transverse, 0.6– 0.85 × as long as broad. Propodeum ( Fig. 53 ) with weak, superficially reticulate or coriaceous sculpture to partly smooth; spiracles of medium size, short-oval, and close to metanotum or separated by less than half smallest diameter. Legs ( Figs 48, 49 ) with meso- and metatibiae entirely testaceous to dark over apical half. Fore wing usually bimaculate ( Fig. 52 ), with infuscate region behind stigmal vein and behind marginal vein basally, but rarely subhyaline.

Description

Female

Body length 1.7–3 mm. Head and mesosoma dark green, with bronze reflections on propodeum ( Figs 48, 51, 53 ). Antenna ( Fig. 54 ) with scape brown to black or testaceous-brown ventrally and towards base; pedicel and flagellum dark brown. Tegula black. Legs ( Figs 48, 49 ) with coxae coloured as body; femora dark with metallic reflections, narrowly testaceous at knees; tibiae whitish-testaceous, protibia with brown stripe at inner surface, meso- and metatibiae pale testaceous and variable darkened at apex, the paler forms being entirely testaceous and darker forms being mostly blackish; protarsus brown, meso- and metatarsi usually with basal two tarsomeres whitish-testaceous and brownish at apex, but sometimes with only basitarsus or three basal tarsomeres pale. Fore wing bimaculate, usually with a brownish area beneath stigmal vein and another brown stripe under proximal end of marginal vein ( Fig. 52 ), but infuscate areas sometimes reduced to almost absent; wing venation pale brownish. Gaster dark brown, with bronze reflections dorsally on basal tergites ( Fig. 48 ).

Head in dorsal view ( Fig. 48 ) 1.1–1.25 × as broad as mesoscutum and 2.3–2.7 × as broad as long; in frontal view transverse-oval, 1.18–1.38 × wider than high; temple reduced, 0.05–0.15 × as long as eye length. POL 1.65–2.1 × OOL, OOL 2–2.8 × OD. Eyes 1.32–1.45 × as high as broad, separated by 0.96–1.15 × their height; eyes almost glabrous, but with very short, sparse hairs. Gena straight to weakly convex, strongly converging, malar space 0.4–0.45 × height of eye. Mouth opening 1.32–1.55 × as broad as malar space. Frons flattened on sides, without piliferous punctures.

Antennae ( Fig. 54 ) inserted with ventral margins of toruli at level of ventral margins of eyes. Scape 5.25– 6.5 × as long as broad, 0.8–0.95 × as long as height of eye, not reaching median ocellus. Pedicel + flagellum 1.15–1.27 × as long as breadth of head, and 1.3–1.55 × as long as breadth of mesoscutum. Pedicel in profile 1.75–2.15 × as long as broad. Funicle with two anelli and three funicular segments, the first anellus laminar, the second discoid; funicular segments decreasing in length, funicle proximally slightly stouter (1.15–1.4 ×) than pedicel, distally very slightly thickened (F3 1.13– 1.3 × as broad as F1) and slightly compressed; F1 distinctly longer (1.6–2.1 ×) than pedicel; F1–F3 2.55– 3.4, 2–2.45, and 1.65–2.15 × as long as broad, respectively. Clava three-segmented, acute apically; 2.8–3.5 × as long as broad; slightly broader (1–1.13 ×) than F3 and 0.8– 0.95 × as long as F2 + F3; compact or with shallow constriction between C1 and C2; C1 1.15–1.47 × as long as broad and 0.4–0.45 × length of clava. Flagellum with sensilla usually placed in three irregular rows, rarely in two or four rows on F1 and F2, in two or rarely three irregular rows on F3, and in two rows on C1 and C2; with short, dense, decumbent, setae.

Mesosoma in dorsal view ( Fig. 48 ) 1.47–1.7 × as long as broad, mesosoma, in lateral view ( Fig. 49 ) weakly convex dorsally, 1.73–1.95 × as long as high with propodeum sloping at about 40–45° with respect to plane of mesoscutum and scutellum. Pronotum 0.2–0.3 × as long as mesoscutum. Mesoscutum transverse, 1.5– 1.63 × as broad as long, and 1.2–1.4 × as long as scutellum; moderately strongly reticulate. Scutellum convex, 0.95–1.05 × as long as broad, with two pairs of strong dark setae; sculpture of scutellum and axillae finer than and not as strong as mesoscutum, the scutellum anterior with slightly elongate sculpture. Dorsellum reticulate ( Fig. 51 ) or coriaceous. Propodeum ( Figs 51, 53 ) medially 1.5–1.83 × as long as dorsellum and 0.43– 0.52 × as long as scutellum; with weak, superficial reticulations or coriaceous but almost smooth towards nucha and behind plical carina, and sometimes with smooth areas on median panels; with fine median carina reaching 0.5–0.75 × its length; plical carina indistinct, indicated only posteriorly; callus with long, white setae; spiracles of medium size, short-oval, separated from metanotum by 0.3–0.5 × smallest diameter.

Fore wing ( Fig. 52 ) 2.3–2.45 × as long as broad. Costal cell 1.07–1.23 × as long as marginal vein and 8–9.3 × as long as broad; ventrally with a complete row of setae and some sparse setae apically, and dorsally usually with a short row of three to six or rarely up to eight setae apically. Submarginal vein dorsally usually with 12–15 but rarely up to 18 setae. Marginal vein 2.9– 3.6 × as long as stigmal vein. Stigmal vein at an angle of 37–44° to the costal wing margin, moderately thin basally; stigma elongate, hardly thickened. Postmarginal vein 1.35–1.7 × as long as stigmal vein and 0.43– 0.55 × as long as marginal vein. Basal fold pilose, rarely with only one or two but usually with three to eight setae; basal cell open behind, bare dorsally and ventrally. Speculum of moderate size, reaching almost to base of marginal vein, rarely almost open but usually closed posteriorly by sparse to dense setae; speculum not effaced at lower surface. Fore wing with moderately dense, dark pilosity beyond speculum; marginal fringe short. Hind wing rounded at apex.

Gaster ( Figs 48, 49 ) ovate, 1.9–2.4 × as long as broad, 1.2–1.5 × as long as mesosoma, 0.95–1.2 × as long as head plus mesosoma, and 0.95–1.13 × as broad as mesosoma; acute apically with syntergum transverse, 0.6–0.85 × as long as broad; tergite T1 with posterior margin convex, reaching 0.2–0.25 × length of gaster. Ovipositor slightly protruding; cercal setae of similar length, not reaching apex of ovipositor. Hypopygium reaching 0.3–0.4 × length of gaster.

Male ( Fig. 50 )

Similar to female except in structure of antennae and gaster, and hyaline wings. Body length 1.2–1.9 mm. Antenna ( Fig. 56 ) with scape 3.5–4 × as long as broad, sensorial area ( Fig. 55 ) wide and pale, reaching 0.4 × width of scape, with 20–26 relatively large sensorial pores densely placed in one irregular row, the interspaces smaller than pore size, and usually some pores arranged in a second irregular row, the pores extending between basal 0.23–0.27 and apical 0.76–0.78 of the length of scape. Pedicel + flagellum 1.45–1.6 × as long as breadth of head and 1.75–1.85 × as long as breadth of mesoscutum. Flagellum with one laminar anellus, four funicular segments, and three-segmented clava; F4 1.25–1.65 × as long as F3 and 0.75–1.05 × as long as clava. Funicle with three long, thin, subcylindrical rami on F1–F3, with long, hair-like setae; funicular segments and all three rami with mps, but denser on all sides of R2 and R3, and sparsely on frontal surface of R1. Fore wing with marginal vein 2.8– 3.25 × as long as stigmal vein; stigmal vein at an angle of 40–45° to the costal wing margin; postmarginal vein 1.45–1.75 × as long as stigmal vein and 0.52–0.6 × as long as marginal vein. Costal cell dorsally with a short marginal row of three to six setae apically. Legs ( Fig. 50 ) variably darkened with mesotibia usually pale or sometimes dark in apical 0.5; metatibia usually dark in apical 0.3–0.5 or sometimes pale, the dark portions brown to pale brown; tarsi with one or two basal tarsomeres pale. Gaster 2–2.9 × as long as broad, 0.9–1.2 × as long as mesosoma, and 0.7–0.95 × as long as head plus mesosoma.

Variation

Variation exists in the extent of leg darkening, depending on distribution, body size, and possibly on winter/ summer generations. Usually the meso- and metatibiae are whitish-testaceous, with only the metatibia darkened pale brown in the apical 0.2–0.3. The fore wings of this form have moderately intense infuscate areas. However, some specimens have darker legs with up to 0.2–0.6 or rarely 0.9 of the mesotibia apically blackish and 0.35–0.5 or rarely 0.7 of the metatibia apically blackish, and sometimes also darker fore wing infuscation. Paler forms occur in southern areas in which the tibiae are almost entirely whitish-testaceous, only slightly darkened apically on the inner side, and usually having fore wings with less intense infuscate areas or with only one slightly infuscate area behind the stigmal vein, to almost entirely hyaline. These paler forms usually also have the basal fold and the cubital fold behind the speculum less setose, with the speculum almost open posteriorly and on the inner side, although sometimes as setose as in darker forms. Variation in antennal segment proportions occurs in small or dwarf specimens, with less distinctly elongate flagellar segments; dwarf specimens also have darker coloured tibiae.

Hosts

Tuta absoluta on Solanum lycopersicum , based on sequenced specimens. No native host is known. The records published as Necremnus sp. nr artynes , and most of the records published as N. artynes in previous surveys of Tuta parasitoids ( Desneux et al., 2010; Ferracini et al., 2012; Zappalà et al., 2012, 2013; Gabarra et al., 2014) belong to N. tutae . The records of N. metalarus parasitizing T. absoluta in Spain ( Urbaneja et al., 2012; Zappalà et al., 2013) probably also refer to dark forms of N. tutae , as for a similar specimen seen from Algeria.

Discussion

Necremnus tutae belongs to the N. artynes group of species based on females having bimaculate fore wings ( Fig. 54 ), an elongate mesosoma and gaster ( Fig. 48 ), relatively long postmarginal vein, and elongate funicle segments ( Fig. 54 ). They are similar to N. artynes in having the propodeum ( Fig. 53 ) weakly reticulate or coriaceous to partly smooth, the spiracles oval and placed near the metanotum, and the meso- and metatibiae variably darkened apically ( Figs 48, 49 ). Although the differences are small, they are confirmed by the molecular results. Females also resemble those of N. navonei , the differences detailed in the description of the latter species. Females of N. tutae differ from N. artynes mainly in the shape of the gaster (1.9– 2.4 × vs. 2.6–3.15 × as long as broad, 1.2–1.5 × vs. 1.5– 1.9 × as long as mesosoma, and 1–1.2 × vs. 1.2–1.4 × as long as rest of body) compared with N. artynes . When the gaster is collapsed it can appear narrower than its natural shape (appearing 2.6–3.2 × as long as broad), but its other proportions with the mesosoma and rest of body are maintained. Additionally, in females of N. tutae the syntergum is distinctly transverse, 0.6– 0.85 × as long as broad, compared with usually slightly elongate or barely transverse, 0.9–1.3 × as long as broad in N. artynes . Males of N. tutae are very similar to those of N. artynes , differing in the scape having a broader sensorial area with the sensorial pores of larger size and densely placed in one irregular row such that the interspaces are smaller than pore size, and usually with some pores arranged in a second irregular row ( Fig. 55 ). In males of N. artynes the sensorial area is narrow and although the sensorial pores are placed in one row they are smaller such that they are separated by interspaces greater than a pore width ( Fig. 15 ). In addition, males of N. tutae have a longer marginal vein, 2.8–3.25 × compared with 2.4–2.7 × as long as the stigmal vein in N. artynes , and the postmarginal vein is frequently longer, 1.45–1.75 × compared with 1.3–1.65 × as long as the stigmal vein in N. artynes .

Atypical small females of N. tutae with dark legs also resemble N. metalarus , being similar in shape of the gaster and the tibiae being partly to almost entirely blackish. However, they differ in having weak, superficially reticulate or coriaceous sculpture on the propodeum and indistinct plical carinae ( Fig. 53 ). The propodeum in N. metalarus is strongly reticulate and the plical carinae are distinct ( Fig. 37 ). Colour of the tibiae and the fore wings are also usually different in typical N. tutae , with the meso- and metatibiae mainly pale testaceous, only darkened apically ( Figs 48, 49 ), and the fore wings bimaculate ( Fig. 52 ). In N. metalarus the meso- and metatibiae are usually dark brown from the base to the apex ( Figs 27 , 32 ) (rarely basal third testaceous), and the fore wings have only one dark area behind the stigmal vein ( Fig. 29 ) (usually faint, but sometimes darker with indication of a second dark area behind the base of marginal vein). Consequently, colour similarities exist only in atypical specimens of both species.

Females of N. tutae with subhyaline wings can also resemble atypical specimens of N. cosmopterix that have pale tibiae, particularly because both species have the same host, T. absoluta . Differences are detailed in the description of the latter species, although females of N. tutae have at least some traces of fore wing infuscation behind the stigmal vein, whereas those of N. cosmopterix have entirely hyaline wings. Typical female N. cosmopterix also have entirely dark tibiae.

Figures

Figures 48–56. Necremnus tutae sp. nov. 48–50, habitus: 48, ♀ dorsal; 49, ♀ lateral; 50, ♂ lateral. 51, ♀ dorsal mesosoma. 52, ♀ fore wing. 53, ♀ metanotum and propodeum. 54, ♀ antenna. 55, ♂ pedicel and scape. 56, ♂ antenna.

Figures 8–16. Necremnus artynes. 8–10, habitus: 8, ♀ lateral; 9, ♂ lateral; 10, ♀ dorsal. 11, ♀ dorsal mesosoma (2012- 5). 12, ♀ fore wing. 13, ♀ metanotum and propodeum (2012-5). 14, ♀ antenna. 15, ♂ pedicel and scape. 16, ♂ antenna.

Figures 32–39. Necremnus metalarus. 32–34, habitus: 32, ♀ lateral (2012-9); 33, ♂ lateral (2012-12); 34, ♀ dorsal (2012- 8). 35, ♀ dorsal mesosoma (2012-8). 36, ♀ fore wings (2012-9). 37, ♀ metanotum and propodeum (2012-8). 38, ♀ antenna (2012-9). 39, ♂ antenna (2012-10).

Figures 26–31. Necremnus metalarus, ♀ lectotype. 26, dorsal habitus; 27, lateral habitus; 28, tegula (arrow); 29, fore wing; 30; head and antenna; 31, metanotum and propodeum.