Necremnus artynes, (WALKER)

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 : 366-371

NECREMNUS ARTYNES (WALKER) ( FIGS 2–16 )

Eulophus Artynes Walker, 1839: 163–164 . ♀ lectotype (BMNH, here designated).

Eulophus subcontiguus Thomson, 1878: 231–232 . ♀ lectotype (LUZN) designated by Boucˇek (1959: 150). Synonymy under N. artynes by Boucˇek (1959: 150).

Type material

Walker (1839) described Eulophus artynes based on at least five females, the description including also four varieties, from material collected on the Isle of Wight, Devon, Cornwall, and Holywood, near Belfast, Northern Ireland. Boucˇek (1959) stated that he saw one female syntype deposited in Berlin, whereas the BMNH has four females indicated to form part of the type series. One point-mounted female has the following six labels: (1) a circular, purple-bordered label with ‘LECTOTYPE’; (2) a rectangular, handwritten label with what appears to be ‘v. 1 [?] w.’; (3) a rectangular label with ‘ Eulophus Artynes Walker’ handwritten on one side and ‘Stood under this name in old B.M. Coll. C. Waterhouse’ printed on the other side; (4) a rectangular, handwritten label with ‘ E. artynes W. Lectotype M. de V. G. ’; (5) a rectangular label with ‘ Eulophus Artynes Walker LECTOTYPE: ♀ M. de V. Graham det. 1958’ partly printed and handwritten; and (6) a square label with ‘ B.M. TYPE HYM. 5.2502’. This female lacks antennae except for the scape of the right antenna, the tarsi of both hind legs and the right middle leg, the tibia and tarsus of the left middle leg, and all wings except for most of the left fore wing. The other three females have circular, blue-bordered labels with ‘PARALECTOTYPE’ as well as the double-sided label. One of these is card-mounted and also has a rectangular, handwritten label with ‘ Artynes ’ and a printed label with ‘ Walker coll. 1904–120’. It lacks its head, some leg parts, and the gaster, although the right antenna and part of the left antenna are glued to the card. The other two are point-mounted. One has a circular label with ‘38/7.12/64’ on three separate lines and a small rectangular label with ‘ Britain’ handwritten; it lacks its head and antennae. The third female labelled as paralectotype lacks labels other than the ‘PARALECTOTYPE’ and the double-sided label, although it has a rectangular card pinned below the specimen to help protect it. It is the only entire specimen .

The initial description for E. artynes states that the apices of the mesotibiae are reddish-yellow (fulvae) and those of the metatibiae are dark (fusci), whereas variety β was described as having the mesotibia dark basally and apically, variety γ as having the mesotibia dark apically and the metatibiae black (nigrae) apically, and variety δ as having the mesotibiae black apically. Leg colour was not described for variety ε, which was simply described as having the first antennal article (scape) reddish-yellow, dark above. The mesotibiae of the female labelled ‘Britain’ are entirely yellow, whereas the metatibiae are essentially entirely yellow, with only the extreme apices being very slightly darker reddishbrown and thus might be variety ε. None of the other three specimens has the mesotibia dark both basally and apically and thus none fits the description of variety β. The other three females have both the meso- and metatibiae quite obviously infuscate apically, although the mesotibia is lighter and somewhat less extensively brownish apically than is the metatibia, the apical darker region of the metatibia encompassing 0.4 of its length. Consequently, the difference between the original description of the legs of E. artynes and those of varieties γ and δ is mostly an appreciation of whether apically the mesotibia is reddish-yellow, dark, or black, which may have altered over time in one or more specimens because of fading. Females comprising the type series do differ noticeably in propodeal sculpture. The female that Graham labelled as lectotype has the propodeum quite shiny with subeffaced, mesh-like sculpture anteriorly and posteromesally, and more distinctly although shallowly reticulate between about the level of the spiracle and propodeal foramen posteriorly ( Fig. 7 ). The female labelled as ‘ Artynes ’ also has a finely sculptured propodeum. However, the entire female has the propodeum finely sculptured and shiny only anterolaterally mesal to the spiracle; otherwise it is distinctly reticulate mesally, behind about the width of the dorsellum, and posterolaterally ( Figs 5, 6 ). The female with the ‘Britain’ label is the only one with distinct plical carinae extending from the propodeal foramen obliquely toward each spiracle. The region lateral to each plical carina is distinctly reticulate whereas the region mesal to the plical carinae is more finely sculptured, although partly shallowly reticulate to coriaceous-reticulate.

Graham did not validly designate a lectotype through publication under ICZN rules and the original description does not describe the propodeal sculpture. Therefore, in order to stabilize the concept of the name, we designate the only complete female ( Figs 2, 3 ) as the lectotype of E. artynes (the one lacking labels except for the double-sided label and Graham’s paralectotype label). We have added a rectangular, red lectotype label to this female and labelled the others with yellow paralectotype labels.

Although Bouček (1959: 150) did not explicitly state that he was designating the lectotype of E. subcontiguus , he stated that he examined ‘the lectotype of Eulophus subcontiguus Thomson’ and provided sufficient details on the condition of the specimen that it could be recognized, which is sufficient to validate the specimen as lectotype. Hansson (1991) subsequently published a separate lectotype designation in order to validate a lectotype designation label by M. de V. Graham on a female. That female bears a printed label ‘Lund’ and has the LUZN type number 1619:1. We did not examine the lectotype, but according to Boucˇek (1959: 150) it lacks its gaster and both antennae beyond the pedicel and ‘is doubtless the same as the syntype of E. artynes Walk. mentioned above’.

Boucˇek & Askew (1968) stated that Necremnus comptus Gahan, 1941 , described from North America (California), probably was a synonym of N. artynes . Unfortunately, the single type female is badly preserved with only the legs remaining. New material and molecular comparisons are needed prior to any formal synonymy.

Redescription

Female

Body length 2–3.1 mm. Head and mesosoma dark green or sometimes with bluish reflections ( Figs 8, 10 ), mainly at sides, or with bronze reflections on propodeum ( Fig. 13 ), and a small anterolateral part of axillae ochraceous. Antenna with scape brown to black or testaceous-brown ventrally and towards base ( Fig. 14 ); pedicel and flagellum dark brown. Tegula black. Legs ( Figs 8, 10 ) with coxae coloured as body; femora dark with metallic reflections, narrowly testaceous at knees; tibiae whitish-testaceous, protibia with brown stripe on inner surface, meso- and metatibiae pale testaceous and variably darkened apically, the paler forms being entirely testaceous and darker forms being blackish in apical half; protarsus brown, meso- and metatarsi sometimes with only basal tarsomeres pale, but usually basal two tarsomeres whitish-testaceous with apices brownish. Fore wing bimaculate ( Figs 2 , 12 ), usually with a brownish area behind stigmal vein reaching half width of disc and another brown stripe behind proximal end of marginal vein reaching cubital row of setae, although infuscate areas sometimes reduced or almost absent with only a faint stigmal infuscation; wing venation pale brownish. Gaster dark brown with bronze reflections dorsally on basal tergite ( Fig. 10 ).

Head in dorsal view 1.15–1.25 × as broad as mesoscutum and 2.3–2.7 × as broad as long; in frontal view ( Fig. 4 ) transverse-oval, 1.3–1.4 × wider than high; temple 0.05–0.18 × as long as eye length. POL 1.65– 2.2 × OOL, OOL 1.9–2.8 × OD. Eyes 1.3–1.43 × as high as broad, separated by 1–1.2 × their height, with very short, sparse hairs. Gena straight to weakly convex, strongly converging, malar space 0.4–0.48 × height of eye, malar sulcus present. Mouth opening 1.2–1.6 × as broad as malar space. Frons flattened on sides, weakly reticulate, with very short hairs, without piliferous punctures. Scrobes depressed, with a median longitudinal carina within scrobal depression. Vertex with short, black setae, occiput densely pilose.

Antennae ( Fig. 14 ) inserted with ventral margins of toruli at level of ventral margins of eyes ( Fig. 4 ). Scape 5–6.5 × as long as broad, 0.83–0.9 × as long as height of eye, not reaching median ocellus. Pedicel + flagellum 1.2–1.3 × as long as breadth of head ( Fig. 4 ) and 1.4–1.65 × as long as breadth of mesoscutum. Pedicel in profile 1.65–2.05 × as long as broad. Funicle with two anelli and three funicular segments, the first anellus laminar, the second discoidal; funicular segments decreasing in length, funicle proximally slightly (1.2– 1.43 ×) stouter than pedicel, distally very slightly thickened (F3 1.2–1.3 × as broad as F1) and slightly compressed; F1 distinctly longer [(1.45)1.8–2.15 ×] than pedicel; F1–F3 (2.35)2.6–3.2 ×, (1.85)2–2.4 ×, and (1.5)1.7–2 × as long as broad, respectively. Clava threesegmented, acute apically; 2.8–3.5(4) × as long as broad; slightly broader (1–1.08 ×) than F3 and 0.8–0.9 × as long as F2 + F3; with shallow constriction between C1 and C2; C1 1.15–1.6 × as long as broad and 0.4– 0.45 × length of clava. Flagellum with sensilla moderately numerous, placed in three or rarely four irregular 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 ( Figs 10, 11 ) 1.5–1.8 × as long as broad, in lateral view ( Fig. 8 ) weakly convex dorsally, 1.7–1.9 × as long as high with propodeum sloping at about 35–45° with respect to plane of mesoscutum and scutellum. Pronotum 0.2–0.35 × as long as mesoscutum. Mesoscutum transverse, 1.45– 1.65 × as broad as long, and 1.15–1.4 × as long as scutellum; notauli visible in anterior half only; slightly shiny, moderately strongly reticulate with isodiametric reticulations; setae sparse, dark, short, and strong. Scutellum convex, 0.95–1.1 × as long as broad, with two pairs of strong, dark setae; sculpture of scutellum and axillae finer and not as strong as mesoscutum, the scutellum anteriorly with slightly elongate sculpture. Dorsellum ( Figs 6, 7 ) reticulate or coriaceous ( Fig. 13 ). Prepectus strongly reticulate. Legs of moderate length and thickness. Propodeum medially 1.4– 1.7 × as long as dorsellum and 0.43–0.5 × as long as scutellum; coriaceous ( Fig. 13 ) or with weak, superficial reticulations ( Fig. 6 ), but almost smooth towards nucha and below plical carina, and sometimes with smooth areas on median panels ( Figs 7 , 13 ); with fine median carina reaching 0.5–0.8 × its length; plical carina indistinct, visible only posteriorly; callus with long, white setae; spiracles of medium size, short-oval, separated from metanotum by 0.3–0.7 × smallest diameter ( Figs 6, 7 , 13 ).

Fore wing ( Fig. 12 ) 2.4–2.6 × as long as broad. Costal cell 1.05–1.2 × as long as marginal vein and 8–9.5 × as long as broad; ventrally with a complete row of setae and some sparse setae apically, and dorsally with a short row of four to eight setae apically. Submarginal vein dorsally with 13–17 setae. Marginal vein 2.8– 3.45(3.55) × as long as stigmal vein. Stigmal vein at an angle of 34–38° to the costal wing margin, moderately thin basally; stigma elongate, hardly thickened. Postmarginal vein 1.4–1.65 × as long as stigmal vein and 0.42–0.55 × as long as marginal vein. Basal fold pilose; basal cell open posteriorly, bare dorsally and ventrally. Speculum of moderate size, reaching almost to base of marginal vein, closed posteriorly. Cubital row of setae slightly sinuate upward behind speculum; subcubital row of setae in one partial row behind speculum. Admarginal row of setae behind marginal vein with one row of long hairs. Fore wing with moderately dense, dark pilosity beyond speculum; marginal fringe short. Hind wing rounded at apex.

Gaster lanceolate ( Figs 2 , 10 ), 2.6–3.15 × as long as broad, 1.5–1.9 × as long as mesosoma, 1.2–1.4 × as long as head plus mesosoma, and 0.85–1.1 × as broad as mesosoma; acute apically with syntergum usually elongate or barely transverse, 0.9–1.3 × as long as broad; T1 with posterior margin convex, reaching 0.15– 0.2 × length of gaster. Ovipositor slightly protruding; cercal setae of similar length, not reaching apex of ovipositor. Hypopygium reaching 0.25–0.35 × length of gaster.

Male ( Fig. 9 )

Similar to female except in structure of antennae and gaster, and hyaline wings. Body length 1.5–2.2 mm. Antenna ( Fig. 16 ) with scape 3.5–4.5 × as long as broad, sensorial area ( Fig. 15 ) narrow, at margin, with 16– 19 small sensorial pores placed in one row extending between basal 0.27–0.3 and apical 0.75–0.83 length of scape, and with interspaces greater than pore size. Pedicel + flagellum 1.35–1.55 × as long as breadth of head and 1.55–1.9 × as long as breadth of mesoscutum. Flagellum with one laminar anellus, four funicular segments, and three-segmented clava, with C1 large, reaching 0.6 × length of clava, and C3 reduced apically. Funicular segments increasing in length, F4 1.35– 1.45 × as long as F3 and 0.8–0.9 × as long as clava. Funicle with three long, thin, subcylindrical rami on F1–F3, the rami, 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 2.4–2.7 × as long as stigmal vein; stigmal vein at an angle of 37–42° to the costal wing margin; postmarginal vein 1.3– 1.65 × as long as stigmal vein and 0.5–0.6 × as long as marginal vein. Costal cell dorsally with a short marginal row of four to six setae apically. Legs ( Fig. 9 ) with mesotibia usually pale or sometimes darkened in apical half, metatibia usually with apical 0.2–0.3 or sometimes up to apical half darkened, with dark portions brown to pale brown, or rarely meso- and metatibiae entirely dark; tarsi usually with basal two but rarely only basal tarsomeres pale. Gaster 2–2.8 × as long as broad, 1.1–1.33 × as long as mesosoma, and 0.85– 1.05 × as long as head plus mesosoma.

Variation

Variation exists in the amount of leg darkening and fore wing infuscation, depending on distribution, body size, and possibly on seasonal generations. In the type material from England and some specimens from France and Spain the mesotibia is entirely pale, and the apical half of the metatibia is dark ( Fig. 3 ) . Other specimens from the same countries have either paler or darker tibiae. Paler forms, frequently in Spain, have the metatibia almost entirely pale with only the apical 0.15–0.3 dark. Darker forms, more frequently in England or France, have the apical half or rarely the mesotibia almost entirely dark. Variation also exists in colour pattern of the fore wings with more or less intense infuscation, and the number of pale basal tarsal segments. Usually the basal two tarsomeres are pale, but sometimes only the basitarsus is pale in small or darker specimens. Antennal segment proportions differ in small or dwarf specimens, these having less distinctly elongate flagellar segments, given in parentheses in the text .

Distribution

Europe ( Noyes, 2013). A record from North America requiring confirmation refers to N. comptus as a possible synonym of N. artynes (Boucˇek & Askew, 1968).

Hosts

Tuta absoluta on Solanum lycopersicum L., and Ap. anthyllidella on Astragalus spp. (Fabaceae) based on sequenced specimens. Some specimens came from lab culture on T. absoluta ; one female emerged from Astragalus stella Gouan together with Ap. anthyllidella , and one male emerged from Astragalus sesameus L., possibly associated also with Ap. anthyllidella . Another host record based on a specimen in R. R. Askew’s collection is Ap. anthyllidella on Anthyllis vulneraria L. (Penbryn, Cardigan, Wales, vi.1979, leg. A. N. B. Simpson). Noyes (2013) also listed Cos. pulchrimella Chambers; however, this is incorrect and is instead the host for one of the cryptic species that we describe, N. cosmopterix . Noyes (2013) also listed Vulcaniella pomposella (Zeller) (Cosmopterigidae) on Salvia aethiops L.; however, according to Koster & Sinev (2003), the true host may be Vulcaniella cognatella Riedl based on the host plant being Salvia . In this case, the species status of the parasitoid requires confirmation.

Discussion

Necremnus artynes is the typical species of the N. artynes group, females having bimaculate fore wings ( Figs 2 , 12 ), an elongate mesosoma and gaster ( Fig. 10 ), relatively long postmarginal vein, and elongate funicle segments ( Figs 4 , 14 ). Within this group, N. metalarus and related species are differentiated by their comparatively coarsely sculptured, reticulate propodeum and dorsellum ( Figs 31 , 37 ), in combination with almost entirely dark metatibia ( Figs 27 , 32 ). Of the species with a weakly reticulate or coriaceous propodeum ( Figs 45 , 53 ), N. artynes most closely resembles N. tutae and N. navonei , the former being misidentified frequently in previous surveys of Tuta parasitoids. The main diagnostic feature for females of N. artynes is the comparatively elongate lanceolate gaster, being 2.6– 3.15 × as long as broad. This is clearly longer than for females of N. tutae (1.9–2.4 ×, Fig. 48 ), although not always for females of N. navonei , which have the gaster 2.35–2.8 × as long as broad ( Fig. 42 ). When the gaster is collapsed in air-dried specimens, it can appear narrower than its natural shape, but its other proportions with the mesosoma and rest of the body are maintained. The gaster is 1.5–1.9 × as long as the mesosoma in N. artynes vs. 1.2–1.5 × in N. tutae and 1.45–1.55 × in N. navonei . Another feature typical of N. artynes females is that the last gastral tergite is usually elongate or barely transverse, 0.9–1.3 × as long as broad, whereas it is clearly transverse, 0.6–0.85 × as long as broad in females of the other species. Other small differences and those of males are detailed in the descriptions of N. tutae and N. navonei .

We sequenced seven females and four males from France and Spain, but not from type localities in England. Specimens from France are the most similar to the type material. Two females ( NA114 , NA147) have typical bifasciate fore wing patterns, the mesotibia essentially entirely yellow, and the metatibia with only about the apical quarter brownish. The other three females ( NA148–150 ) have both the mesotibia and metatibia with up to or slightly more than the apical half brown, but only NA150 has a typical fore wing pattern, the other two either having a superficially hyaline fore wing ( NA149 ) or with only a faint brownish region behind the stigmal vein ( NA150 ) .

Figures

Figures 2–7. Necremnus artynes. 2–6, lectotype ♀: 2, dorsal habitus; 3, lateral habitus; 4, head and antenna; 5, dorsal mesosoma; 6, metanotum and propodeum. 7, paralectotype ♀: metanotum and propodeum.

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 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.

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 40–47. Necremnus navonei sp. nov. 40–42, habitus: 40, ♀ lateral; 41, ♂ lateral; 42, ♀ dorsal (2013-65). 43–46, ♀ (2013-65): 43, fore wing; 44, dorsal mesosoma; 45, metanotum and propodeum; 46, antenna. 47, ♂ antenna (2013-66).

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.