Micrurapteryx caraganella (Hering, 1957) Hering, 1957

Kirichenko, Natalia, Triberti, Paolo, Mutanen, Marko, Magnoux, Emmanuelle, Landry, Jean-Francois & Lopez-Vaamonde, Carlos, 2016, Systematics and biology of some species of Micrurapteryx Spuler (Lepidoptera, Gracillariidae) from the Holarctic Region, with re-description of M. caraganella (Hering) from Siberia, ZooKeys 579, pp. 99-156 : 108-117

Taxon classification Animalia Lepidoptera Gracillariidae

Micrurapteryx caraganella (Hering, 1957) comb. n. Figs 4, 5, 14, 19, 26, 27, 42, 43, 49-54, 55-58, 65-76, Suppl. material 4: S35, S36

Citations.

[ Parectopa sp.; Hering 1957: 230]

[ Parectopa caraganella Hering 1957: 1122. Type locality: Central Siberia]

[ Parectopa caraginella ; Dovnar-Zapol’skiy 1969: 36, subsequent incorrect spelling; Tomilova 1973: 8]

[ Gracilaria caraganella ; Dovnar-Zapol’skiy and Tomilova 1978: 34]

[ Micrurapteryx gradatella ; Kuznetzov 1981: 177, figs 173, 3-4; Kuznetzov and Tristan 1985: 189, figs 15-17; Noreika 1997: 380, figs 257-258; Kuznetzov and Baryshnikova 1998: 5-6; Kuznetzov 1999: 21, figs 3-4; misidentifications]

Material examined.

Adult (18): 1 ♂ Caragana arborescens , Krasnoyarsk, Akademgorodok, Yenisei bank 12.07.2013, N. Kirichenko, Kr-19-13-1, slide TRB3995♂; 1♀, 1 ex abdomen missing, Caragana arborescens , Krasnoyarsk, Akademgorodok, Yenisei bank 12.07.2013, N. Kirichenko, Kr-19-13-/2/4, TRB3986♀; 4 ♀, 1 ex abdomen missing, Caragana arborescens , Krasnoyarsk, Akademgorodok, Yenisei river bank, 18.08.2014, N. Kirichenko, slide TRB4061; 2 ♂, Caragana arborescens , Krasnoyarsk, Akademgorodok, Yenisei river bank, 18.08.2014, N. Kirichenko, slides MIC6940, MIC6941 (CNC); 1♂, 2♀, Caragana arborescens , Novosibirsk: SCBG SB RAS, 02.07.2013, N. Kirichenko, Nov-19-13-1/2/3, slide TRB3994♂, TRB 4052♀; 2♀, Caragana arborescens , Krasnoyarsk, Akademgorodok, Yenisei bank, 15.07.2014, E. Akulov; 2 ♂, Russia, Siberia, Omsk (Victory park), Caragana abrorescens , 23.VII.2015, reared from mines, N. Kirichenko, slides NK-186-15-1, NK-186-15-2; 2 ♂, Russia, Siberia, Omsk (Victory park), Caragana frutex , 23.VII.2015, reared from mines, N. Kirichenko, slides NK-184-15-1, NK-184-15-2; 1 ♀, Russia, Siberia, Omsk (Victory park), Caragana frutex , 23.VII.2015, reared from mines, N. Kirichenko, slide NK-184-15.

Pupa (6): Caragana arborescens , Micrurapteryx sp., Russia, Krasnoyarsk, Akademgorodok, Yenisei river bank, 11.07.2013, N. Kirichenko, Kr-26-13. Larva (12): 5 larvae of the tissue-feeding instars, labelled as above, 12.07.2013, N. Kirichenko, Kr-19-13, 1 larva, Caragana boisii , Russia, Novosibirsk: SCBG SB RAS, 06.06.2012, N. Kirichenko, 22-12; 1 larva, Caragana arborescens , Russia, Novosibirsk: SCBG SB RAS, 03.08.2011, N. Kirichenko, Kr-30-11; 1 larva, Caragana arborescens , Russia, Omsk: Victory park, 23.VII.2015, N. Kirichenko, NK-186-15; 1 larva, Caragana frutex , Russia, Omsk: Victory park, 23.VII.2015, N. Kirichenko, NK-184-15; 1 larva, Caragana arborescens , Russia, Tyumen: Zatyumenskiy park, 24.VII.2015, N. Kirichenko, NK-209-15; 1 larva, Caragana arborescens , Russia, Tobolsk: Ermak garden, 25.VII.2015, N. Kirichenko, NK-212-15; 1 larva, Caragana arborescens , Russia, Barnaul: Izymrudniy park, 27.VII.2015, N. Kirichenko, NK-223-15.

Nomenclatural availability of Parectopa caraganella Hering, 1957.

The binomen Parectopa caraganella was first used by Hering (1957: 1122) who attributed it to Danilevsky without further indication. In his three-volume work, Hering (1957) distinguished the larva of a species of Parectopa from that of Phytagromyza caraganae E. Rodendorf (now Aulagromyza caraganae (Hering, 1957), see Ellis 2015) ( Diptera , Agromyzidae ), both being leaf miners on Caragana in Siberia. In his key on p 230 of volume 1, Hering wrote " Parectopa sp." for species #1100a with the following "Anfangsgang us. lang, epidermal. Kot im Platz teilweise ausgeworfen. Larva mit Kopfkapsel und Beinen … 1100a. Parectopa sp. (Lept.) Unterseite Gang seicht, weisslich. Oberseite Platz beginnt auf der Mittelrippe, kann das ganze Blättchen einnehmen, dieses und Mine gewechselt (Europa). 7,8 Central-Siberien (Buhr)" (= "Beginning of mine on underside, long, epidermal. Frass partially ejected from mine. Larva with head capsule and legs … 1100a. Parectopa sp. (Lept.) Underside tunnel/gallery shallow, whitish. Upperside blotch begins on the midrib, can take the whole leaflet, this (e.g. the leaflet), and mine can be changed (Europe) 7,8. Central Siberia (Buhr)."). Thus Hering “described” the larva and its mine, albeit in an extremely minimalist way but sufficiently to distinguish it from the next taxon. The fact that the latter is a fly is irrelevant. Hering did not use the name caraganella on page 230. However, in volume 2 of the same publication (published simultaneously) on p 1122, in reference to volume 1, he listed a number of corrections. Thus page 1122 contains the following entry: "p. 230, Nr. 1100a: Parectopa caraganella Danilevsky (statt Parectopa sp.)" ["instead of Parectopa sp."]. Again in the index on p 1164 Hering listed " Parectopa caraganella Danilevsky Suppl. 1100a": the reference to entry #1100a undisputably links the taxon name to the description in the key of p 230.

Hering’s distinction in a key constitutes, however unintentionally, a valid description and thus makes the name Parectopa caraganella nomenclaturally available with Hering as the author. Despite being woefully inadequate, the “description” provided in Hering’s key minimally meets the criteria expressed in Article 13.1.1 of the Code, namely that a name published after 1930 (but before 1960) "be accompanied by a description of definition that states in words characters that are purported to differentiate the taxon" ( International Commission on Zoological Nomenclature 1999).

It is worth noting that the description of the mine in association with the host plant provides a more useful diagnosis in the present case. Because the mine constitutes the work of an animal it could be construed as a condition for availability (Code article 12.2.8). However, such evidence is not admissible to assess the availability of names published after 1930.

Given its year of publication, a type specimen is not even required. Did Hering have voucher material of that species from Siberia when he wrote his 1957 work? He only mentioned the name “Buhr” at the end of the key couplet, who is presumably the person who communicated the information to him. He did not indicate how he obtained the name he attributed to Danilevsky. Even if so, the existence of voucher specimens would not affect the attribution of the name to Hering.

In a catalogue of leaf-mining insects, Dovnar-Zapol’skiy (1969) cited " Parectopa caraginella Dan." (this seems to be a misspelling of caraganella ) as a species feeding on Caragana described by Danilevsky from Western Siberia without any further reference or indication. As such, that citation has no nomenclatural value.

Kuznetzov and Tristan (1985) correctly discounted the names Parectopa caraganella Danilevsky and Parectopa caraginella Danilevsky as nomenclaturally unavailable. Indeed, despite being cited by several authors, no original publication by Danilevsky where either spelling of the name is mentioned seems to exist. It is intriguing that no authors who cited or attributed the names to Danilevsky gave any indication or reference where those names were seen in the first place.

Diagnosis.

The forewing pattern of Micrurapteryx caraganella is very similar to that of Micrurapteryx gradatella and the two species are separable with certainty only by examination of the genitalia. In male genitalia, Micrurapteryx caraganella differs mainly by the presence of a sharp, prominent tooth on the middle of the ventral margin of the valva. This character allows distinguishing easily this species from all other congeners. In female genitalia, the antrum is ampulla-shaped with lateral broadenings, whereas it is almost cylindrical in Micrurapteryx gradatella . The cremaster differs in pupae of the two species: there are three pairs of little spines in Micrurapteryx gradatella ( Patočka and Turčáni 2005) versus five pairs in the new Micrurapteryx caraganella . The larva of Micrurapteryx caraganella differs modestly from those of Micrurapteryx gradatella and Micrurapteryx kollariella by the enlargements of the internal margins of the dorsal apodemes, along the epicranial notch.

Description of adult

(Figs 4, 5). Wing span 8.7-10.2 mm.

Head. Frons and vertex white, sometimes sprinkled with brownish grey. Palpi white; labial palpus rather long and slender, upturned, with apically forked dark brown band on median segment and sometimes apical one ringed with grey; maxillary palpus slightly more than half length of apical segment of labial palpus, spotted with fuscous outside. Antenna as in Micrurapteryx gradatella .

Thorax. Legs and thorax as in Micrurapteryx gradatella . Forewing dark brown in ground colour with white markings; costal margin with 5 white strigulae, the first four curving outwards, the fifth inwards, the first long and strongly oblique, the fourth often indistinct; dorsal margin with basal ⅔ white, this fascia denticulate inwards, often linked irregularly with costal strigulae; apical spot black with some mixture of paler scales, surrounded by circular white line including 5th costal strigula; cilia and hindwing as in Micrurapteryx gradatella .

Abdomen. Brownish grey dorsally and white ventrally, apical segment with lateral dark grey spot in the female. Segment 7 of male similar to Micrurapteryx gradatella . Sternum 6 of female as in gradatella but posterior margin more rounded.

Male genitalia (Figs 26, 27). Tegumen short, triangular at apex, with no setae; tuba analis membraneous, without subscaphium, produced beyond tegumen, very similar to Micrurapteryx gradatella . Valva longitudinally cleft, costal region with sinuous margin, cucullus lobe rounded; sacculus with large, sharp tooth in middle of ventral margin and apex ventrally produced into strongly sclerotized toothed process with two pointed ends. Phallus tubular, about 0.9x length of valva, slightly bent in apical third, with small broadenings at base, a few small teeth on medio-ventral and dorsoapical walls and 2-3 larger denticles before apex; vesica with rather large patch of microspines and a thin, long cornutus apically pointed. Segment 7 with a pair of coremata of thin scales almost as long as width of sternum.

Female genitalia (Figs 42, 43). Anal papillae rather short, posterior apophyses shorter than anterior ones. Segment 8 about same length as anal papillae, weakly sclerotized. Sternum 7 markedly sclerotized, elongate-conical. Ostium bursae wide and rounded. Antrum sclerotized, ampulla-shaped, with lateral broadenings; inception of ductus seminalis near its anterior end; distal third of ductus bursae broadened, strongly and irregularly sclerotized with elongate-papillate microsculpture, medial third with thin lateral sclerotized band and proximal one completely membraneous. Bursa copulatrix slender, with pair of opposite signa each as cluster of 3-5 long spines. Ductus spermathecae with efferent canal forming 4 or 5 wide coils before vesicle (not shown). Segment 6 equal to preceding ones, sternum strongly sclerotized, posterior margin convexely rounded.

Pupa

(Figs 49-54). Maximum length 4.2 mm; width 0.9 mm. Head setae as in Micrurapteryx gradatella . Frontal process (cocoon cutter) a transverse ridge strongly and irregularly dentate. Antenna extended to abdominal segment A7, A8 or A10; forewing to A5, A6 or A7; hindleg from posterior margin of A7 to just beyond apex of abdomen. Setae D1, SD1 and L1 present on abdominal segment A1-7. Cremaster consisting of ring of five pairs of small recurved spines, two dorsal pairs slightly enlarged and more closely set, ventral pair very small.

Larva

(Figs 55-58). Tissue-feeding form examined of presumed last instar.

Head. Frons elongate, extended to epicranial notch, dorsal apodemes well developed, margins of epicranial notch with slight enlargement, on each side of caudal half while in Micrurapteryx gradatella these margins are regular; chaetotaxy with all three MD setae present, P2 very reduced; six stemmata on each side, arranged in 2 groups: first with 1 ventrad to A3, 2 between S2 and A3, 3, ventrad, near S2; second group in oblique line close to antenna. Mandible with 4 dorsal teeth and two ventral; both lateral setae present.

Body. Cuticle densely covered with very minute hairs, except on pronotal plate and small, symmetrical areas; chaetotaxy rather similar to that of Acrocercops -group ( Kumata 1988): L setae bisetose on all segments except A9, SV bisetose on T1 and unisetose on T2-3, proprioceptor MD1 and MV3 present on T2-3 and A1-9; prolegs on A3-5 and A10. Most setae are inconspicuous, particularly the D and SV groups.

Biology

(Figs 65-76). The species usually mines the leaves of Caragana arborescens (Figs 65-69) but some individuals (i.e. larvae in mines) were also found on Caragana frutex (Figs 70-71), Caragana boisii ( Fabaceae ) (Figs 73, 74) and on the herbaceous Medicago sativa ( Fabaceae ) (Fig. 72). The mine is a roundish or slightly branched blotch (branches are short, 2-5 mm long) above the midrib (Figs 68-69). Often a long, narrow tunnel is visible on the lower surface of the leaf (Fig. 71). The mine quickly develops into an upper-surface flat blotch with digitate channels, occupying half or an entire leaflet (Figs 68, 69, 72, 73), similar to Micrurapteryx gradatella (Figs 59-62). Fresh mines are white (Figs 66-72) with larvae visible when examining the mines with backlighting (Figs 73). The larva consumes all layers of palisade parenchyma and partly damages the layers of spongy parenchyma. Since not all spongy parenchyma is eaten, the colour of the mine can be slightly greenish yellow. Larvae eject frass out of the mine by protruding the rear end of their body through a slit (up to 7 mm long) on the underside of leaves. Larvae can leave their mines (Fig. 74) and begin a new one, either on the same or a neighboring leaflet.

Pupation (Figs 75-76). Pupation takes place outside the mine, usually on the lower surface of a leaflet where the larva spins a transparent, glossy cocoon, locating it usually perpendicular to the midrib, as in case of Micrurapteryx gradatella (Figs 63-64). Silk deposition by the prepupa induces a slight buckle in the leaf so that presence of the cocoon can be detected from above by the curved appearance of the leaflet. Occasionally pupation may also occur on the upper side of a leaflet, at the base along the midrib (Fig. 75).

Phenology.

In Siberia, Micrurapteryx caraganella has two generations. The overwintering stage is not known (but is likely to be as a pupa or adult); neonate larvae of the first generation usually occur in early June. Adults fly in early July. The second generation develops from mid-July until the end of August.

Ecology and host plant range.

Leaf mines of the new species were most commonly found in Siberia on Siberian peashrub, Caragana arborescens ( Fabaceae ), a plant widely used for different purposes: as an ornamental, for erosion control, as a source of nectar for bees, and for nitrogen fixation ( Shortt and Vamosi 2012). Caragana arborescens is native to Siberia, China, Mongolia, and Kazakhstan ( Yingxin et al. 2010). In North America, where the shrub was introduced in 1752, it is naturalized and widespread ( Shortt and Vamosi 2012).

Dovnar-Zapol’skiy and Tomilova (1978) mentioned Vicia sp. as a host plant for Parectopa caraginella / Gracilaria caraganella . Their record likely refers another Micrurapteryx species, particularly Micrurapteryx gradatella which is known to develop on Vicia sepium in Europe ( Ellis 2015) and, according to our observations, on Vicia amoena in Siberia.

NK looked for mines of Micrurapteryx on Vicia spp. plants growing in the same locality as Caragana arborescens with mines of Micrurapteryx caraganella . No mines of Micrurapteryx caraganella were found on this herbaceous vetch, whereas leaf mines were common on Caragana arborescens . In Krasnoyarsk, on Vicia , particularly Vicia amoena NK recorded mines of Micrurapteryx gradatella .

These findings suggest that Micrurapteryx caraganella is an oligophagous insect with a preference for Caragana arborescens . In the Central Siberian garden SB RAS (Novosibirsk) in July 2012, NK also found a few mines of Micrurapteryx caraganella on Caragana boisii , an allied plant originating from China. In July 2015 in Omsk (Victory park), NK recorded mines of Micrurapteryx caraganella on Caragana frutex (native in Siberia). In the same location and at the same time bushes of Caragana arborescens were observed to be heavily attacked by Micrurapteryx caraganella (Figs 66, 67), whereas bushes of Caragana frutex growing in vicinity (20 m from the damaged Caragana arborescens ) were hardly colonized by the insect. In Omsk, on the same plot, NK also found the occasional mines of Micrurapteryx caraganella on the herbaceous legume Medicago sativa growing near heavily infested Siberia peashrub Caragana arborescens .

Distribution.

Siberian regions previously considered part of the range of Micrurapteryx gradatella , namely Tyumen, Omsk, Kemerovo, Novosibirsk, Irkutsk oblats, Altai krai ( Sinev 2008), the Republics of Buryatia and Yakutia (Sakha) ( Dovnar-Zapol’skiy and Tomilova 1978), where it was recorded feeding on Caragana , most likely refer to caraganella . In July-August 2015, NK recorded Micrurapteryx caraganella at these locations, except in Kemerovo and Yakutia. Additionally, NK found it in the south of Krasnoyarsk krai and in the easternmost corner of Siberia, Transbaikal krai, in Chita (Victory Park). Also the reports of Micrurapteryx gradatella from Tajikistan and the Russian Far East (see above) probably belong to Micrurapteryx caraganella . There are no records of Micrurapteryx caraganella for North America where its host plant Caragana arborescens has been introduced as an ornamental.