Micrurapteryx baranchikovi Kirichenko, Akulov & Triberti, 2021

Kirichenko, Natalia I., Akulov, Evgeny N., Triberti, Paolo & Belokobylskij, Sergey A., 2021, A new species of Micrurapteryx (Lepidoptera, Gracillariidae) feeding on Thermopsis lanceolata (Fabaceae) in southern Siberia and its hymenopterous parasitoids, ZooKeys 1061, pp. 131-163 : 131

Micrurapteryx baranchikovi Kirichenko, Akulov & Triberti sp. nov.

Type material.

Holotype ♂ (Fig. 4A, B): Republic of Khakassia, near the Black Lake field station of SIF SB RAS, along the lake bank, Thermopsis lanceolata ; 28.VII.2020 coll. (mine), N. Kirichenko & E. Akulov coll, 08.XII.2020 emerged (hereafter indicated as em.), field no. NK-08.12-1 (♂), genitalia slide NK-08.12-1♂, DNA barcoded (Process ID: GPRU015-21) (SIF). Paratypes. 15♂, 35♀ (Fig. 4C-F). Republic of Khakassia, near the Black Lake field station of SIF SB RAS, along the lake bank, Thermopsis lanceolata , 28.VII.2020 coll. (mine), Kirichenko N. coll., 14.I.2021 em., field no. NK-11-3, genitalia slide TRB4429♂ (MSNV); same label, but 17.I.2021 em. (from 2 mines), field nos NK-9-2, NK-10-3, genitalia slide TRB4425♀, TRB4428♂ (MSNV); 18.I.2021 em., field no. NK-11-4, genitalia slide TRB4430♀ (MSNV); 27.VII.2020 coll. (2 mines), 22.I.2021 em. 2♂, field nos NK-13-1 (♂), NK-13-3 (♂) (SIF); same label, but N. Kirichenko & E. Akulov coll., 28.VII.2020 coll. (mine), 26.XI.2020 em., field no. NK-26.11-1 (♀), genitalia slide NK-26.11-1♀ (SIF), DNA barcoded (Process ID: GPRU018-21); same label but 08.XII.2020 em., field no. NK-08.12-2 (♂), genitalia slide NK-08.12-2♀ (SIF), DNA barcoded (Process ID: GPRU017-21); same label but 29.XI.2020 em., field no. NK-29.11-1 (♀), genitalia slide NK-29.11-1♀, (SIF), DNA barcoded (Process ID: GPRU016-21); same label but 27.VII.2020 coll. (mine), 7.I.2021 em. 2♀, field nos NK-13-2 (♀), NK-10-1 (♀); same label but 28.VII.2020 coll. (mine), 24.XII.2020 em., field no. NK-11-1 (♀); 30.XII.2020 em., field no. NK-12-1 (♀);same label but 2.I.2021 em. 2♀, field nos NK-16-1 (♀), NK-11-5(♀); same label but 3.I.2021 em., 2♀, field nos NK-9-1 (♀), NK-12-3 (♀), genitalia slide NK-12-3♀; same label but 15.I.2021 em., field no. NK-10-2 (♀); same label but 19.I.2021 em., field no. NK-10-4 (♀); same label but 28.VII.2020 coll. (mine), 14.XI.2020 em. 4♀ & 1♂, field nos NK-14.11-1 (♀), NK-14.11-2 (♀), NK-14.11-3 (♀), NK-14.11-5 (♀), NK-14.11-4 (♂), genitalia slides NK-14.11-1♀, NK-14.11-2♀; same label but 26.XI.2020 em., field no. NK-08.12-3 (♀); same label but 3.XII.2020 em., field no. NK-03.12-1 (♀), genitalia slide NK-03.12-1♀; same label but 7.XII.2020 em. 3♀ & 1♂, field nos NK-07.12-1 (♀), NK-07.12-2 (♀), NK-07.12-3 (♀), NK-07.12-4(♂), genitalia slide NK-07.12-4♂; same label but 8.XII.2020 em., field no. NK-08.12-3 (♂); 15.XII.2020 em. 1♀ & 2♂, field nos NK-15.12-1 (♀), NK-15.12-2 (♂), NK-15.12-3 (♂); same label but 17.XII.2020 em. 3♀ & 1♂, field nos NK-17.12-1 (♀), NK-17.12-2 (♀), NK-17.12-3 (♀), NK-17.12-4 (♂); same label but 20.XII.2020 em. 2♂ & 2♀, field nos NK-20.12-1 (♂), NK-20.12-3 (♂), NK-20.12-2 (♀), NK-20.12-4 (♀), genitalia slide NK-20.12-2♀; same label but 25.XII.2020 em. 1♀ & 1♂, field nos NK-25.12-1 (♀), NK-25.12-2 (♂); same label but 26.XII.2020 em. 1♂ & 2♀, field nos NK-26.12-1 (♂), NK-26.12-2 (♀), NK-26.12-3 (♀), genitalia slide NK-26.12-3♀; 27.XII.2020 em. 1♂ & 2♀, field no. NK-27.12-1 (♂) (SIF).

Additional material examined.

Pupa (2): Republic of Khakassia, near the Black Lake field station SIF SB RAS, along the lake bank, Thermopsis lanceolata , 28.VII.2020 coll. (2 mines), Kirichenko N. coll., field nos NK-28-1, NK-28-2. Larva (4): same label, (mine), filed no. Kh-NK-20-1, DNA barcoded (Process ID: GPRU044-21); same label but 27.VII.2020 coll. (2 mines), field nos NK-27-1, NK-27-2; same republic but Belyo Lake, along the lake bank, 7.VII.2020 coll. (mine), Kirichenko N. coll., filed no. Kh-NK-20-2, DNA barcoded (Process ID: GPRU045-21).

Diagnosis

(Figs 4, 5). The forewing pattern of M. baranchikovi reflects the typical habits of the genus: a series of costal strigulae, a white band along the dorsal margin and a projection of the fringe line at apex (Fig. 4B-F). However, the genital structures allow easy identification. The male genitalia of M. baranchikovi are distinguished from congeners by the pointed and not rounded valvar tip (Fig. 5A, B). This character is present only in M. sophorivora Kuznetzov & Tristan, 1985 (Fig. 5E), which is widely distributed in central western Asia and whose larvae feed on Sophora and Robinia ( Fabaceae ) (Seven and Genҫer 2009; De Prins and De Prins 2021). The two species are separable by the following characters in the male genitalia: (1) different inclination of the valvar and saccular apices with respect to the horizontal axis of the valvae, at 90° in M. sophorivora versus at ca. 45° in M. baranchikovi ; (2) straight phallus with a single and elongate cornutus, coremata wider and shorter than half phallus in M. sophorivora versus somewhat curved phallus, no cornuti, coremata longer than half phallus and thin in M. baranchikovi (Fig. 5A-E).

In the female genitalia, the differences are the following: thin ductus bursae and piriform corpus bursae with a group of thorn-like signa in M. sophorivora , while in M. baranchikovi ductus and corpus bursae are not differentiated and signa mostly absent or reduced to ca. ten microspines (Fig. 6A, D). These characters are present in the female genitalia of M. salicifoliella , but this species is easy distinguishable by the sclerotised section of antrum / ductus bursae protruding from the anterior margin of segment 7 (S7) (Kirichenko et al. 2016). The male genitalia of M. baranchikovi are very different from those of M. salicifoliella (see figs 28-29 in Kirichenko et al. 2016).

Description of adult

(Figs 4-6). Male and female. Alar expanse 8.0-11.0 mm (51 specimens).

Head. Frons, vertex and palpi white with intermixture of dark scales around eyes. Labial palpus rather long and slender, slightly upturned; maxillary palpus ca. half of apical article of labial palpus. Antenna fuscous dorsally, scape, pedicel and ¼ of flagellum white ventrally, remaining articles ringed with paler colour; pecten absent.

Thorax. Dorsum white, ventral side and tegulae brownish grey. Legs white, fore, mid coxae and femurs dark brown outwardly, tibiae and tarsi annulated and of the same colour. Wing venation as in M. kollariella (see Vári 1961). Forewing dark brown in ground colour with white markings; costal margin with five white strigulae. First three strigulae almost parallel, oblique and bent outwards. First strigula very dilated on the costal margin and projected backwards, second often obsolescent, last two semi-circular, often both touching opposite margin or, in some specimens, fused apically. Fifth strigula with a dark apical dot. Dorsal margin white in basal 4/5 with two thin, linear projections distally, sometimes not connected to white margin. Cilia white around apex to tornus with dark brown tips interrupted by linear marking protruding from fringe line (not from dark apical dot). Hindwing grey ochreous, cilia pale grey.

Abdomen. Entirely brownish grey, last segments white ventrally, wider in male compared to female. A pair of thin coremata in the intersegmental membrane S5/S6, ca. half the width of S6 (Fig. 5C). S8 weakly sclerotised, tergum reduced to thin, narrow transverse band. In the female S6 shorter than or equal to preceding one and ca. a quarter of S7 long, sternum sclerotised, anterior margin with slight medial convexity (Fig. 6F).

Male genitalia. Tegumen short, subtriangular at apex, with long and thin pedunculi; tuba analis long and membranous, produced beyond tegumen, without suscaphium but with a pair of lateral lamellae, with no setae. Valva longitudinally cleft, costal region slightly concave, apex of cucullus pointed and inclined 45° with respect to longitudinal axis of valva; sacculus markedly developed, rectangular, apex produced into a pointed process with toothed margins, downward-oriented and almost parallel to cucullus (Fig. 5A, B). Phallus ca. 0.9 times length of valva, flattened, base bifurcate, longitudinally a thin, mid-ventral toothed crest and a long, lateral thickening ending before a pointed apex, no cornuti (Fig. 5A, B, D).

Female genitalia. Posterior apophyses not spine-shaped but lamellar, anterior ones longer, linear, and thin. S8 short, ca. same length as posterior apophysis, weakly sclerotised. S7 ca. four times S8 long, sternum markedly sclerotised, elongate subrectangular, its posterior margin modified in a membranous sector provided with a row of long and thin scales. This structure, supported by a sclerotised transverse bar, delimits a wide sinus vaginalis where, ventrally, the ostium bursae opens; opening of ostium is ca. half the width of S7 (Fig. 6E). Antrum and posterior section of ductus bursae undifferentiated, with dorsal wall strongly sclerotised for a length of just over half of S7 and covered with microspinules while the ventral one, membranous, bears a thin longitudinal thickening. Inception of ductus seminalis at anterior end of sclerotised section. Ductus and corpus bursae undifferentiated, signa mostly absent or reduced to ca. ten microspines. Ductus spermathecae with efferent canal forming three coils before vesicle (not shown).

Variability

(Fig. 6). The new species exhibits considerable diversity in the structures of the bursa copulatrix. In most examined specimens (seven out of ten), ductus and corpus bursae are undifferentiated (Fig. 6A), in three other specimens, the ductus is narrower than corpus bursa (Fig. 6B, C). It could be due to individual variability; another explanation could be related to the method of dissection, in particular boiling, resulting in contraction of ductus in its apical part.

Another issue are microspines in the corpus bursae that were recorded in ca. half of all dissected females. In those females, two opposite weakly sclerotised plates containing ca. ten microspines were present, often hardly visible (Fig. 6C, D). Nevertheless, the adults with such variability did not differ in other morphological characters. The two females were DNA barcoded: one without microspines and another one with microspines in the corpus bursae (Fig. 6B, C); they showed very low genetic divergence (0.3%), leaving no doubt that they are one species.

Taxonomic remarks.

Since it is still uncertain whether there is a separate Thermopsis -feeding species in North America “”, here we examine the possibility that it could be conspecific with M. baranchikovi . To do this, we compared the Chambers’s original description of Parectopa thermopsella (Chambers 1875) with that of M. baranchikovi . In the genus Micrurapteryx , habitus is quite uniform and indistinguishable for many species (Kirichenko et al. 2016); therefore, any particular character can be important for species differentiation. We detected specific characters in adult morphology allowing to distinguish between " Parectopa " Parectopa thermopsella and M. baranchikovi . These characters are listed below, with the original description of Parectopa thermopsella 's characters italicised and provided word-by-word as it appeared in Chambers (1875), followed by the indication of differences in M. baranchikovi :

(1) " Outer surface of the second joint of the palpi dark gray brown, inner surface white, third joint whitish with a brownish annulus before the tip. " In M. baranchikovi , labial palpi entirely white.

(2) " Antennae dark gray brown annulated with white. " In M. baranchikovi , antennae with scape, pedicel and part of flagellum white ventrally, remaining articles ringed with paler colour.

(3) " The dark brown of the disc is divided into three distinct spots by three short white streaks emitted from the white dorsal margin, and which pass a little obliquely backwards, the first placed before the middle, the second about the middle and the third behind it. " These markings are absent in the new species.

(4) " In the grayish part of the wing are five white costal streaks; the first of these is long and narrow, beginning about the basal third of the wing length and passing obliquely backwards until it almost touches the white of the dorsal margin in the apical part of the wing, the second is wider and much shorter, the third shorter and narrower than the second, but both oblique; while the fourth is still shorter, and is nearly perpendicular to the margin. " In M. baranchikovi , the first streak is very dilated on the costal margin and projected backwards, while the third and fourth are well developed and almost similar, always wider than the second, which is almost obsolescent.

Larva.

(Fig. 7A, C, E). The studied last instar larvae are tissue-feeders. The larva is yellow. It probably develops in five instars. The morphology does not show particular differences from M. caraganella (Kirichenko et al. 2016).

Pupa.

(Figs 7B, D, F, 8). The young pupa is yellow, soon turns brownish; length 4.5-5.0 mm, width 0.7-1.0 mm. Frontal process (cocoon cutter) simple with pointed projection (Fig. 8); clypeal setae paired, very reduced and nearly contiguous; antenna and hindleg extended to S8; forewing to S5. Setae D1, L1 and SD1 present on S1-S7. Cremaster is very similar to M. caraganella (Kirichenko et al. 2016) consisting of a ring of five pairs of small spines, dorsal pair slightly enlarged, the two most ventral pairs are the smallest.

Etymology.

The species is named in honour of Dr. Yuri N. Baranchikov, Russian forest entomologist and scientific supervisor of NK and EA, in recognition of his research in regional Lepidoptera and his effective 30-year heading the Black Lake field station of the V.N. Sukachev Institute of Forest SB RAS in Khakassia, around which the new Micrurapteryx species was discovered.

Bionomics

(Figs 7G-M, 9). In Khakassia, M. baranchikovi develops in one generation annually. Adults are on wing in late May to early June. Oviposition takes place from early to mid-June. Eggs are laid on the lower surface of the leaves. Early instar larvae are found in the mines in late June to early July; late instar larvae in late July to early August. Pupation from early to late August; the pupae hibernate.

The mine (Fig. 9A) is similar to that of other Micrurapteryx species (Kirichenko et al. 2016). It starts on a lower side of the leaf (rarely on stipules) as a relatively long contorted well-visible tunnel in the epidermis (Fig. 9B). Soon the larva continues its development in a roundish or slightly branched blotch mine situated above the midrib of a leaflet (Fig. 9C, D). Older mines can occupy almost the complete leaflet (Fig. 9A). If several mines occur per leaflet, enlarging blotch mines merge and several larvae are found in one mine. Initially blotch mines are pale green, later yellowish or whitish. Severely damaged plants turn white (Fig. 9E, F); damaged leaves with abandoned mines soon turn brown and desiccate.

The blotch mines are nearly free of frass; larvae eject frass grains outside the mine by protruding the rear part of the body through a coarse slit that they gnaw in the lower epidermis. Often, frass can be found next to the slit; a few frass grains can be still seen inside the mines. Older larvae are able to vacate the mine and start a new one on a neighbouring leaflet or leaf by making a cut in the lower epidermis of leaf lamina and rapidly biting into the mesophyll.

Pupation is external. The larva vacates the mine and moves to a neighbour or a distant leaf, where it spins a relatively thick cocoon (Fig. 7G). Most often pupation takes place on the lower side of the leaf lamina along the midrib (Fig. 7H). The colour and the shape of the cocoon resembles the midrib, making it difficult to spot the cocoon. In dense populations, the pupation may occur in other places: on the upper side of the leaf next to the leaf edge, in the basis of the leaf (Fig. 7J), exceptionally inside the mine (Fig. 7K) or on a legume surface (Fig. 7L). The thick cocoon seems to help pupae to overwinter in the steppe with little or no snow cover. After adult emergence, the pupal exuviae (i.e., the 2/3 of its length) protrude through the opening of the cocoon (the least dense part of the cocoon) (Fig. 7M). In 2020, under laboratory conditions, the adults started emerging in ca. two weeks after they were moved from the fridge (where they overwintered for two month at a temperature of +3 °C) to room conditions (temperature + 23 °C, humidity 70%), and the emergence lasted for ca. one month.

Host plant.

The host plant is the perennial legume herb, the lanceolate bush-pea, Thermopsis lanceolata ( Fabaceae ). The name T. lanceolata was proposed in 1811 by R. Brown for the plant from Siberia which was mistakenly determined in 1803 by P. Pallas under the name of Sophora lupinoides L. (Zhu and Kirkbride 2005). Thermopsis lanceolata grows in the steppe with chernozemic solonetzic and sandy soil, on stony and gravelly slopes, in meadows and agricultural fields, along lakes and rivers, as well as on disturbed areas and in/around settlements (Tolmachev 1974; Telyatiev 1985).

The plant is poisonous due to the high concentration of alkaloids (Telyatiev 1985). However, these alkaloids also make it a medical herb (Volynskiy et al. 1978). In Russia, the antitussive drugs produced from T. lanceolata have been utilised for decades to treat tracheitis, bronchitis and pneumonia (Telyatiev 1985; Lager 1988; Vidal Handbook 2021). Furthermore, the alcaloid cytisine extracted from T. lanceolata is a major component of respiratory analeptic drag against asphyxia (Telyatiev 1985). Finally, this alkaloid is also used for treating nicotine addiction (Telyatiev 1985; West et al. 2011; Hajek et al. 2013). Thermopsis lanceolata was reported to be weedy in some parts of Russia (Telyatiev 1985). Getting into hay, it can poison livestock, in particular horses (Telyatiev 1985; Minaeva 1991).

Distribution.

The leaf mines of Micrurapteryx baranchikovi were found in the steppe area of the Republic of Khakassia (south-western Siberia) in two localities: around Black Lake (in 5 km from the Black Lake field station of SIF SB RA) and next to Belyo Lake (beach “Majorca”). The sampling area is situated in a temperate climatic zone (Grigoryev and Budyko 1960). Summers are dry and hot, with a number of sunny days in the republic, higher than in neighbouring regions; winters are cold, with little snow. The average air temperature in July is +18 °C, in January -19 °C (Samoilova et al. 2019). In the steppe area, the average annual precipitation is ca. 250 mm per year; up to 70% of precipitation falls in summer, of which 55% falls in August with rains and showers (Samoilova et al. 2019). The growing season lasts ca. 165 days (Samoilova et al. 2019).

It is highly likely that the moth is distributed across most of the republic where the host plant is present. Also, bearing in mind that T. lanceolata has rather extensive range in the Urals, in some other parts of Western and Eastern Siberia, as well as in Central Asia (Kazakhstan, Kyrgyzstan), Northern China and Mongolia (Kotunkov 1974; Telyatiev 1985; Lager 1988; Wu and Raven 2010), the occurrence of the moth in these regions is quite possible.

Outbreak character.

In July-August 2020, we recorded a local outbreak of the moth in the type locality, covering an area of ca. 500 m2. Up to 15 mines per leaf and up to 57 mines per plant were documented. The damage peak occurred in late July to mid-August, i.e., when the leaf mines reached their maximal size (and some still contained mature larvae) and the abandoned mines turned brown and dried out. Bearing in mind that T. lanceolata is used in Russia for medical purpose, severe damage caused by the new species may locally affect its harvesting in the Republic of Khakassia.

Indoor survival rate.

In 2020, we obtained 53 moths from 300 pupae by indoor rearing; the survival rate of Micrurapteryx baranchikovi (at the pupal stage) was only 17.6% (53/300). Twenty seven out of 247 pupae were parasitised (see next section). The remaining 220 pupae (73.3%) did not succeed to develop to adults after hibernation.

Parasitoids.

Overall, 27 parasitoid adults emerged from 300 pupae of M. baranchikovi , i.e., parasitism level was only 9% in 2020. Under laboratory conditions, the emergence of parasitoids lasted 12 days, from 10th to 21st of August.

The reared parasitoids were identified to three taxa: two braconids, Agathis fuscipennis (Zetterstedt, 1838) ( Agathidinae ) and Illidops subversor (Tobias & Kotenko, 1986) ( Microgastrinae ), and one ichneumonid Campoplex sp. aff. borealis (Zetterstedt, 1838) ( Campopleginae ). The identification of the first two species was done by external morphology; A. fuscipennis was additionally DNA barcoded, however, by its DNA barcode it was determined to genus level only. We failed to provide an exact identification of the Khakassian Campoplex neither by morphology nor by DNA barcoding. Morphologically, the examined specimens showed similarity to Campoplex borealis by colour of hind legs and shape of temple in dorsal view (see taxonomic note below).

All parasitoids reared from M. baranchikovi are solitary species. In our laboratory rearing, A. fuscipennis dominated and accounted for 18 out of 27 parasitoids (i.e., 67% of all emerged parasitoids), followed by Campoplex sp. aff. borealis (6 adults, 22%) and I. subversor (3 adults, 11%). They all represented novel records for the Republic of Khakassia and were documented as parasitoids of Gracillariidae for the first time.