Leptochilus (Euleptochilus) limbiferus ( Morawitz, 1867 )

Fateryga, Alexander V., Popovich, Anton V., Podunay, Yulia A. & Fateryga, Valentina V., 2020, First data on the bionomics of Leptochilus (Euleptochilus) limbiferus (Morawitz 1867) (Hymenoptera: Vespidae: Eumeninae), with taxonomic notes and new records, Zootaxa 4851 (2), pp. 289-304 : 293-298

Leptochilus (Euleptochilus) limbiferus ( Morawitz, 1867)

Odynerus limbiferus Morawitz, 1867: 136 , ♀ ♂ (type locality: “ Dalmatia ” [ Croatia]), lectotype (designated here): ♀, “Dalmatia” [ZISP] ( Figs 1–4 ).

Leptochilus limbiferus anatolicus Blüthgen, 1955: 24 , ♀ (type locality: “ Kawak (SW Samsun, Anatolia)” [ Turkey]); Gusenleitner 1966: 346, Turkey; 2013a: 45, Turkey; Giordani Soika 1970: 63, Turkey; van der Vecht & Fischer 1972: 44, Turkey. New synonymy.

Leptochilus limbiferus limbiferus: Blüthgen 1967: 232 , Bulgaria; Blüthgen & Königsmann 1969: 927, Albania; van der Vecht & Fischer 1972: 44, Balkans; Gusenleitner 1993: 756, Greece, Albania, Bulgaria, Macedonia, Bosnia, Croatia, Slovenia, Italy.

Leptochilus limbiferus achaeus Gusenleitner in Blüthgen & Gusenleitner, 1970: 291–292 , ♀ ♂ (type locality: “Korinth, Peloponnes” [ Greece]); van der Vecht & Fischer 1972: 44, Greece; Gusenleitner 1993: 756, Greece; Fateryga 2017: 9, Russia (Krasnodar Terr.); Fateryga et al. 2017: 34, Russia (Krasnodar Terr.). New synonymy.

Leptochilus limbiferus: Antropov & Fateryga 2017: 185 , Russia (North Caucasus), Europe (Southern, Eastern), Armenia, Turkey.

Remarks. Gusenleitner (1993) recognized three subspecies of Leptochilus limbiferus based on coloration. In our opinion, such a division is unnecessary. For example, subspecies rank was not used in relatively better studied social wasps ( Carpenter 1996; Carpenter & Kojima 1997). In the case of L. limbiferus , the division on subspecies does not work as well. Turkish specimens must have reddish tegula but we examined a female (see below) with whitish one. The coloration of the Azerbaijani specimens (see below) is similar to rather some Balkanian ones than the Turkish one. At the same time, specimens from Russia correspond to L. limbiferus achaeus described from Greece. Therefore, we treat all subspecies names as synonyms.

The record of “ Microdynerus limbiferus F. Mor. ” from Armenia (“ Eriwan ” [= Yerevan]) by Morawitz (1895: 483) repeated by Antropov & Fateryga (2017) was based on a misidentification of Leptochilus duplicatus . There is a female specimen of L. duplicatus with the labels “ Eriwan.”, “к. Ф Моравица” [coll. F Morawitz], and “ limbiferus F. Mor. ♀.” stored in ZISP. It was impossible to find any material on true L. limbiferus from Armenia and thus, this species must be excluded from the Armenian fauna. At the same time, L. duplicatus is new for Armenia and the Caucasus as a whole. It is important that F. Morawitz did not distinguish his species from L. duplicatus . There are also two specimens (♀ and ♂) of L. duplicatus from Nice ( France) in ZISP, which were also labeled by him as L. limbiferus . Therefore, the lectotype of L. limbiferus designated in the present contribution provides taxonomic stability as it is congruent with the current understanding of F. Morawitz’s species. Leptochilus limbiferus can be easily distinguished from L. duplicatus by light spot on dorsal mesepisternum, light bands on scutellum and metanotum, shorter distance between lateral ocellus and occiput, and flat sternum 7 of male.

Material examined. Type material. Lectotype (designated here): Dalmatia, 1 ♀, leg. Erber (full labels are the following: “ Dalmatia Erber. ”, “к. Ф Моравица” [coll. F Morawitz], “ limbiferus . Mor. ♀.”, “typ F. Morawitz det.”, “ Lectotypus N. Kurzenko des. 2000” [yellow label]) [ ZISP] ( Figs 1–4 ); N. V. Kurzenko did not publish this designation . Paralectotype: Dalmatia, 1 ♂ (full labels are the following: “ Dalmatia. ”, “к. Ф Моравица” [coll. F Morawitz], “ limbiferus F. Mor. ♂.”, “typ F. Morawitz det.”, “ Paralectotypus N. Kurzenko des. 2000” [pink label]) [ ZISP] . Additional material. Russia: Krasnodar Terr.: Anapa , 1 km S Varvarovka (44°48′18″N, 37°21′58″E), 19. VI .2014, 1 ♂, leg. M. V . Mokrousov; Anapa, Supsekh (44°51′04″N, 37°20′42″E), 8. VI .2017, 3 ♀, 1 ♂, 16. VI .2019, 1 ♂, leg. A. V . Fateryga ; ibid., on Dorycnium herbaceum , 8. VI .2017, 1 ♂, leg. A. V . Fateryga ; ibid., from nests, 15. V .2019, 1 ♂, 15. VI .2019, 1 ♀, 1 ♂, 18–24. VI .2019, 1 ♀, leg. A. V . Fateryga [ CFUS]; Anapa, Sukko (44°47′N, 37°22′E) , 20.VII.2018, 1 ♂, leg. I.B. Popov; Kanevskoy Distr. , Trud Khutor (46°08′N, 38°31′E) , 13.VII.2018, 1 ♂, leg. I.B. Popov [ CIPK] . Italy: Friuli Venezia Giulia: Trieste, Aurisina , 28.V–8. VI .1970, 2 ♂, leg. E. Bregant [ FSCV] . Croatia: Dalmatia , [18]66, 2 ♀, leg. Erber [ ZISP] . Split-Dalmatia County: Hvar , 12. VI .1962, 1 ♀, leg. J. Gusenleitner [ FSCV] . Dubrovnik-Neretva County: Ragusa [currently Dubrovnik], VI .1926, 1 ♂, leg. Meyer [ ZISP] . Montenegro: Montenegro , [18]67, 2 ♀, leg. Erber [ ZISP] . Romania: Constanţa County: Agigea , 26. V .1968, 1 ♀, 6.VII.1968, 1 ♂, 14.VII.1968, 1 ♂, leg. C. Nagy [ FSCV] . Bulgaria: Burgas Prov.: Sozopol , 9.VIII.1966, 1 ♀, leg. W.J. Pulawski [ FSCV] . Azerbaijan: Nakhchivan Autonomous Republic : Ordubad, Arax [River], 1892, 1 ♀, leg. Reitter [ ZISP] ; Babek, Goynuk , 39°18′N, 45°40′E, 1680 m, 12. VI.2019, 1 ♂, leg. M.Yu. Proshchalykin, Kh.A. Aliyev, M.M. Maharramov [ FSCV] . Turkey: Konya Prov.: Meram , 14. VI .1968, 1 ♀, leg. J. Schmidt [ FSCV]. Country uncertain: 1867, 1 ♂, leg. Erber [ ZISP] .

Distribution. Russia (Krasnodar Terr.), Italy, Slovenia, Croatia, Bosnia and Herzegovina, Montenegro (*new record), Albania, North Macedonia, Greece, Romania, Bulgaria, Azerbaijan (*new record), Turkey. The presence of this species in Ukraine shown in the “Fauna Europaea” database ( Gusenleitner 2013b) is doubtful since it has not been documented by specimen based records. The records from Armenia ( Morawitz 1895; Antropov & Fateryga 2017) are erroneous (see above).

Bionomics. Nesting substrate. The nesting site of Leptochilus limbiferus ( Fig. 5 ) was described above in the “Material and methods”.All 12 nests were located in empty shells of Xeropicta derbentina . The shells with the nests were found hidden in dense grass; i.e., there were no nests in shells lying on a bare ground surface near the vole holes. The orientation of the shell opening was various.

Nesting activity. Two nesting females were observed. The first one was noticed on June 16, 2019 at 16.20 (solar time). That time, it was sealing the nest. The female flew from the nest and landed on a bare ground surface near a vole hole in about 1 m from the nest. Then, it began running over the ground investigating the surface with the antennae. After some time (up to a minute), the female found a small pellet of dry soil, took it with the mandibles, and flew back to the nest. At the nest, it simply put the pellet into the shell opening and flew again. Sometimes, the female spent some time at the nest after delivering an earthen pellet. That time, it rearranged the pellets, which had been already put into the nest. The abovementioned activity repeated many times until the shell opening is filled with such pellets of dry soil. After that, the female began to bring gravel particles instead of earthen pellets. It also took them on the bare ground surface near the vole hole. At the nest, the female usually not simply put them onto the pile of the pellets of dry soil but rearranged some pellets and other gravel particles, which had been already brought. For this purpose, the wasp used mandibles and fore legs ( Fig. 6 ). After a necessary number of the gravel particles had been arranged in the shell opening, the female began sealing slits between them. For this purpose, it licked the earthen pellets, located between the gravel particles, with the proboscis ( Fig. 7 ). A liquid substance exuding from the glossa moistened the pellets of dry soil and bonded them. The bonded soil received in such a way firmed the gravel particles together. Thus, just the outer part of the cell plug was firmed while the earthen pellets located inside remained unbonded. The female finished its work at 18.15 and flew away.

The second nesting female was noticed on June 27, 2019 at 13.35. Its nest was at the provisioning stage but it was invaded by ants (see below). Several times, the female arrived to the nest and flew away but without any works. The observations were finished at 14.45.

Structure of the nests. Nests of Leptochilus limbiferus occupied about 1.5 of the shell volution. All of them consisted of one cell. The incomplete nest invaded by ants contained remains of the nest plug as well as remains of the inner layer of the wasp cocoon served as a cell bottom. It means that the females of L. limbiferus are able to use the shells several times. At the same time, it does not mean that they do not clean the shell prior to use it. The cocoon remains discovered in the abovementioned nest tightly adhered to the shell walls and were hardly removable. There were no loosely lying or not firmly attached remains of the old nest; such materials had been cleaned out by the female.

Complete nests were sealed with the plug. Its outer surface contained gravel particles, shell bits, and sometimes also tiny shells firmed with bonded soil ( Fig. 8 ). A freshly sealed nest contained an egg at the distant end of the cell (approximately in the middle of the second volution of the shell) and the prey in the form of packed small caterpillars. Closer to the shell entrance, the caterpillars were replaced by pellets of dry soil, which lay loosely ( Fig. 9 ). These pellets completely filled the space between the prey and the outer firmed part of the cell plug; there was no empty space in the nest.

The nests with cocoons, however, did not contain the pellets of dry soil; their plugs were represented by the firmed part only ( Fig. 14 ). It was obvious that the pellets were moved from their original position to the basal (inner) part of the cell by the wasp larva. At the same time, they had been crumbled up and transformed to loose soil. One nest contained a double plug consisted of two equal parts made of gravel firmed with bonded soil.

The liquid used by the female wasp to moisten soil probably contained nectar since L. limbiferus was never recorded collecting water. At the same time, the nest plugs were found to contain monosaccharides, an obligatory component of nectar ( Fig. 15A ). The same test with nest partitions of Syneuodynerus egregius provided doubtful result ( Fig. 15B ). The latter species makes mud by mixing dry soil with regurgitated water and probably saliva (Fateryga, unpubl.), which can contain monosaccharides in trace amounts.Anyway, the test with the nest plugs of L. limbiferus was clearly positive, although this species uses an order of magnitude less liquid than S. egregius .

Provision. Caterpillars of three species were stored as the prey. The first nest contained 45 caterpillars ( Fig. 10 ). Among them, 43 belonged to Syncopacma coronillella (Treitschke) ( Lepidoptera : Gelechiidae ). They lived on Dorycnium pentaphyllum subsp. herbaceum and wove its leaves to characteristic clusters. Hunting was not observed but it was obvious that to capture a caterpillar, the female wasp gnawed out a hole in such a leaf cluster ( Fig. 11 ). Two other caterpillars belonged to an unidentified species, probably in the family Psychidae . The incomplete nest invaded by ants contained 25 caterpillars: nine of them were S. coronillella and 16 belonged to another unidentified species, probably also in the family Gelechiidae .

Immature instars and development. One egg of Leptochilus limbiferus was observed; its size was 2.2×0.7 mm ( Fig. 13 ). It was suspended by the female wasp on the cell wall with a filament. When the larva hatched from the egg, it immediately began feeding on the stored prey. After consuming all provisions, it spun a cocoon. While doing this, it firstly moved prey feces and all loosely lying soil from the nest plug to the end of the shell cavity. Some gravel particles could be also moved if they were not firmed ( Fig. 14 ). After that, the larva began spinning the cocoon itself. It consisted of several layers. The outer layer was thin, whitish, and semitransparent; it tightly adhered to the inner walls of the cell except the area where the soil was deposited by the larva. The inner layer was much thicker; it had beige color and was nontransparent. Its volume corresponded to the size of the larva. Lateral walls of the inner cocoon layer were united with the outer layer. Two to three middle layers were present. They looked like almost flat transverse discs located between the nest plug and the cap of the inner layer ( Fig. 14 ). Similarly to the outer layer, the middle layers were thin, whitish, and semitransparent. All layers of the cocoon consisted of silk strands, which had various width; there were no other material embedded to them. The difference of the inner layer from the other ones was mainly its greater thickness ( Fig. 16 ). The middle layers, however, also had larger areas of smooth, presumably airtight films of silk ( Fig. 17 ). The duration of the feeding and the cocooning was not documented. The meconium was located inside the cocoon. After it was discharged onto the bottom of the cell, the larva passed to the prepupal stage and hibernated until the next spring ( Fig. 12 ).

Four nests with the overwintered wasp progeny were dissected on May 15. One of them contained an adult male gnawing the nest plug. Two other ones contained female and male pupae. The wasps emerged from them in June. The fourth nest contained a prepupa. A female emerged from it at the end of June. Unfortunately, the prepupa from the nest found on June 16 died. The species is probably univoltine. According to the data of the studied collections, adult wasps are active up to the beginning of August (see “Material examined”).

Reproductive success. Just four nest cells were successful among 12 studied ones. As noted above, one nest was invaded by ants during the provisioning stage. It was tiny ant of the species Plagiolepis pallescens Forel ( Hymenoptera : Formicidae ). The ants stolen the wasp egg and tore off fragments from the caterpillars stored in the nest. The female wasp was unable to do anything with this due to very small size of the predators. One of the complete nests with dead progeny contained dead pupa of an anthracine fly ( Diptera : Bombyliidae ) inside the wasp cocoon. Six other nests contained progeny dead for the unknown reason (one larva and five prepupae). It could be stated that the reproductive success amounted 33.3% but the age of the six nests was actually unknown. If they were made by wasp females a year earlier than the other studied nests, it would be incorrect to include them in the reproductive success calculation.

Adult feeding. Specimens of Leptochilus limbiferus were observed feeding on nectar at flowers of five plant species in five families. Females were recorded on Tripleurospermum inodorum (L.) Sch. Bip. ( Asteraceae ) ( Fig. 18 ) and Euphorbia seguieriana Neck. ( Euphorbiaceae ). A male was recorded on Asperula supina M. Bieb. (Rubiaceae) . Several males were observed feeding on Dorycnium pentaphyllum subsp. herbaceum . Both females and males of L. limbiferus have rather long proboscis allowing them visiting flowers with nectar hidden inside a corolla tube, such as A. supina . The wasps (both sexes), however, were also revealed feeding at flowers of an undescribed species of Linaria (Plantaginaceae) , which had nectar hidden in the spur, which was much longer than the wasp proboscis. To get the nectar, L. limbiferus gnawed the spur of Linaria sp. with the mandibles and then inserted the proboscis into the resulted hole ( Fig. 19 ).

Unusual behavior of adult wasps (both females and males) was also observed. The wasps landed on a rather dry substrate, which did not contain nectar, extended the proboscis, and licked substrate surface with the glossa. Such substrates were various parts of plants, e.g., petals of Medicago falcata ( Fig. 20 ), fruits of Dorycnium pentaphyllum subsp. herbaceum , rachis of Hedysarum tauricum , as well as a paper notebook, an air cushion ( Fig. 21 ), a stick of an entomological net, human skin, and clothes. It could be supposed that such a behavior served to obtain some mineral substance. The duration of such acts was up to 20–30 min. They were, however, periodically interrupted: wasps flew away but then returned again and repeated their action.

Male behavior. Males were observed mainly patrolling the nesting site. They made slow flights across its territory. Doing this, the males periodically (1–2 times per minute) landed on grass or stones. Such a behavior was sometimes interrupted for feeding on flowers or abovementioned licking various substrates. Three times the males were observed landing on shells of Xeropicta derbentina and investigating them with the antennae. These shells were actually abandoned nests of the wasp since they had remains of the nest plug. A couple of Leptochilus limbiferus was observed once. Courtship lasted 16 min. It might, however, take actually more time because the wasps had been noticed already together ( Fig. 22 ). After that, copulation was observed during few seconds but it was probably unsuccessful. One male was found sleeping inside an empty shell of X. derbentina ( Fig. 23 ) at 17.35 (solar time).

Figures

FIGURE 15. Qualitative test for monosaccharides with α-naphthol (A, aqueous extract of nest plugs of Leptochilus limbiferus; B, aqueous extract of nest partitions of Syneuodynerus egregius; C, aqueous extract of natural clay; D, 0.4% aqueous solution of glucose; E, distilled water); the reddish quinoid compound (arrows), formed at the boundary of the layers of sulfuric acid and the tested solution, indicates the presence of monosaccharides.

FIGURES 1–4. Odynerus limbiferus Morawitz, 1867, ♀, lectotype. 1, habitus in dorsal view. 2, habitus in lateral view. 3, head in frontal view. 4, labels.

FIGURES 5–12. Bionomics of Leptochilus limbiferus. 5, nesting site. 6–7, a female sealing its nest in a shell of Xeropicta derbentina. 8, a sealed shell with a nest. 9, dissected shell with the prey and the pellets of dry soil. 10, prey ejected from one nest. 11, leaves of Dorycnium pentaphyllum subsp. herbaceum woven by a caterpillar of Syncopacma coronillella; the hole is probably made by a female of L. limbiferus. 12, dissected shell with a prepupa hibernating in the cocoon. Scale bars = 1 cm.

FIGURES 13–14. Schematic plan of a nest and the immature instars of Leptochilus limbiferus. 13, an egg. 14, a prepupa in the nest (A, loose soil; B, prey feces; C, gravel particles; D, meconium; E, inner layer of the cocoon; F, outer layer of the cocoon; G, middle layers of the cocoon; H, a tiny shell; I, bonded soil). For clarity, the inner and the outer cocoon layers are shown as detached from the cell walls, whereas in reality they tightly adhere to them in most part of the outer shell walls and on the inner surface of the nest plug.

FIGURES 16–17. SEM micrograph of two cocoon layers of Leptochilus limbiferus (from inside). 16, the inner layer. 17, a middle layer.

FIGURES 18–23. Bionomics of Leptochilus limbiferus. 18, a female feeding on nectar on a capitulum of Tripleurospermum inodorum. 19, a female feeding on nectar from a flower of Linaria sp. through a hole gnawed out by itself in the spur. 20, a male licking the outer surface of the petals of a flower of Medicago falcata. 21, a female licking an air cushion. 22, courtship. 23, a male sleeping in a shell of Xeropicta derbentina.