Three new remarkable species of the genus Endonura Cassagnau, 1979 from the Middle East and Central Asia (Collembola, Neanuridae, Neanurinae, Neanurini)

Abstract New species belonging to the genus Endonura is described and illustrated in detail. Endonura longirostris sp. n., from northern Iran, is distinctive due to an exceptionally elongate buccal cone compared to that of most other species of the genus. Other characteristic features of the species are the white body with pigmented eyes, a reduced chaetotaxy of the lateral part of the head, the thorax II–III and abdomen I–III with free chaetae De2 and 3, and abdomen IV with particularly short chaetae Di1. The main characteristics of Endonura paracentaurea sp. n. include a white body with dark pigmented eyes, a nonogival labrum, the presence of tubercles Di on the first thoracic segment and of microchaetae on the rudimentary furca. Endonura turkmenica sp. n. can be recognized by its bluish-grey body, labral chaetotaxy, free chaetae E on the head, and notably short chaetae De3 on the thorax and the abdomen. Short remarks on the possible importance of labral modifications are also provided.


Introduction
Amongst springtails, primitive and wingless insects, the subfamily Neanurinae is one of the most diversified, widespread, and species-rich systematic units and evolutionary lineages. Up to date, Neanurinae encompasses nearly 800 species, classified into six tribes (Cassagnau 1989). The Neanurini is the second largest tribe within the subfamily, after Paleonurini, currently containing over 170 valid species belonging to 22 genera (Cassagnau 1989, Hopkin 1997, Deharveng and Bedos 2000, Deharveng et al. 2007, Smolis 2007, 2011, Mayvan et al. 2015. The genus considered in this paper, Endonura Cassagnau, 1979, is among the most thoroughly studied and largest genera within the tribe, with 48 valid species at the moment (Dallai 1983, Deharveng 1979, 1982, Fanciulli and Dallai 2008, Pozo and Simón 1981, Smolis and Kaprus' 2003, 2009, Smolis 2008, 2016, 2011, 2016a. Regarding the actual distribution of its members, Endonura is a Holarctic genus, with the highest concentration of forms in Europe. Recent discoveries, however, slowly change this picture as a notable number of newly described species has been recorded in the Middle East, the Caucasus, and Central Asia (Smolis et al. , 2016a. In 2008, the first author redefined Endonura as follows (Smolis 2008): 0-2 ocelli on either side of the head, reduced mouth parts usually with a thin mandible and a styliform maxilla, separate tubercles Di and De on the head, the non-cross-type of chaetotaxy on the head, and three or two tubercles on the penultimate abdominal segment. Amongst Neanurini, the genus is more similar, and presumably seems to be closely related, to two genera: Cryptonura Cassagnau, 1979, andDeutonura Cassagnau, 1979, which share the following characters with Endonura: maximum 2+2 eyes on the head, the non-cross-type of chaetotaxy, and differentiation in size of dorsal chaetae. Nonetheless, Endonura can be separated from the former by having two or three tubercles on the dorsal side of the penultimate abdominal segment (in Cryptonura, four tubercles), and from the latter by the separation of tubercles Di on the head (in Deutonura, fused).
The examination of rich materials of Neanurinae from northern Iran and Turkmenistan has revealed three unknown species of the genus. One of them seems to be particularly remarkable because of an exceptionally elongated and pointed labrum. Descriptions of all the three taxa are provided with comments on their affinities and the significance of labral modifications in the taxonomy and ecology of the genus and the subfamily Neanurinae.
The specimens were cleared in Nesbitt's fluid, subsequently mounted on slides in Swan's medium and studied using a Nikon Eclipse E600 phase contrast microscope. Figures were drawn with camera lucida and prepared for publication using Adobe Photoshop CS3. Etymology. The name longirostris refers to an exceptionally long buccal cone of this species.
Diagnosis. Habitus typical of the genus Endonura. Dorsal tubercles present and well developed. 2+2 pigmented eyes. Buccal cone exceptionally long, labrum ogival. Head with chaetae A, B, C and D. Chaetae O and E absent. Tubercles Cl and Af separate. Tubercles Dl and (L+So) on head with 4 and 8 chaetae respectively. Tubercles Di on Th I absent. Tubercles De on Th II and III with 3 and 4 chaetae respectively. Tubercles L on Abd III and IV with 3 and 5-6 chaetae respectively. Abd IV and V with 8 and 3 tubercles respectively. Claw without inner tooth. Tibiotarsi with chaetae B4 and B5 short.
Description. General. Body length (without antennae): 0.50 (juvenile) to 1.45 mm (holotype: 1.45 mm). Colour of the body white. 2+2 medium black eyes, in a typical arrangement for the genus (one anterior and one posterior eyes, Fig. 4).
Legs. Chaetotaxy of legs as in Table 1c. Claw without internal tooth. On tibiotarsi, chaeta M present and chaetae B4 and B5 relatively short and pointed.
Remarks. Because of the presence of particularly elongated mouthparts and substantial reduction of chaetotaxy on lateral part of head, E. longirostris sp. n. strongly resembles E. cretensis (Ellis, 1976), known to date from Greece (Crete, Ellis 1976) and Israel (Smolis and Kaprus' 2009). Nevertheless, these species can be easily distinguished from each other by the set of characters: body colour (in longirostris white, in cretensis bluish), presence/absence of chaeta O on head (in longirostris absent, in cretensis present), number of labial chaetae (in longirostris ten, in cretensis eight), presence/absence of tubercles Di on Th I (in longirostris absent, in cretensis present), number of ordinary chaetae De on Abd I-III (in longirostris three, in cretensis two) and number of chaetae Di on penultimate abdominal segment (in longirostris 3+3, in cretensis 1-2+1-2).
Viewing the recently published key to Endonura species (Smolis et al. 2016b), E. longirostris sp. n. is placed the nearest to E. saleri Fanciulli et Dallai, 2008, described from northeastern Italy (Fanciulli and Dallai 2008). However, these species differ in a number of details, including: shape of labrum (in longirostris ogival, in saleri nonogival), number of chaetae (L+So) on head (in longirostris eight, in saleri nine), number of chaetae Dl on head (in longirostris four, in saleri five), location of chaetae De 2 on Th II-III (in longirostris free, in saleri connected with tubercle De), location of chaetae De 2 on Abd I-III (in longirostris free, in saleri connected with tubercle De) and length of chaeta Di1 on Abd IV (in longirostris distinctly shorter than chaeta Di1 of Abd V, in saleri slightly shorter than chaeta Di1 of Abd V).
Etymology. The name "paracentaurea" refers to a strong similarity of the new species to E. centaurea. Diagnosis. Habitus typical of the genus Endonura. Dorsal tubercles present and well developed. 2+2 pigmented eyes. Buccal cone short, labrum nonogival. Head with chaetae A, B, C and D. Chaetae O and E absent. Tubercles Cl and Af separate. Tubercles Dl and (L+So) on head with six and eight chaetae respectively. Tubercles Di on Th I present. Tubercles De on Th II and III with three and four chaetae respectively. Tubercles L on Abd III and IV with three and six chaetae respectively. Abd IV and V with eight and three tubercles respectively. Claw without inner tooth. Tibiotarsi with chaetae B4 and B5 short.
Antennae. Typical of the genus. Dorsal chaetotaxy of Ant III-IV as in Fig. 11 and Table 2b. S-chaetae of Ant IV of medium length and moderately thickened, S4 and S7 notably longer than other S-chaetae, S1 distinctly shorter and thinner than others (Fig. 11). Apical vesicle poorly developed, unilobate. Ventral chaetotaxy of Ant III-IV as in Fig. 12 and Table 2b.
Legs. Chaetotaxy of legs as in Table 1C. Claw without internal tooth. On tibiotarsi, chaeta M present and chaetae B4 and B5 relatively short and pointed.
Remarks. Morphologically, E. paracentaurea sp. n. strongly recalls E. centaurea Cassagnau et Péja, 1979, a form shortly described from Greece (Cassagnau and Péja 1979) and recently redescribed (Smolis 2016). Both species are characterised in having white body, same number of chaetae on tubercles Dl and Af on head, same number of dorsal chaetae on Th and Abd and microchaetae on furca rudimentary. Nevertheless, the new species can be recognised by presence of pigment on eyes (in centaurea absent), Etymology. The name turkmenica is derived from Turkmenistan, the name of the country where the species was found.
Diagnosis. Habitus typical of the genus Endonura. Dorsal tubercles present and well developed. 2+2 pigmented eyes. Buccal cone relatively long, labrum ogival. Head with chaetae A, B, C, D and E. Chaeta O absent. Tubercles Cl and Af separate. Tubercles Dl and (L+So) on head with six and eight chaetae respectively. Tubercles Di on Th I absent. Tubercles De on Th II and III with three and four chaetae respectively. Tubercles L on Abd III and IV with three and six chaetae respectively. Abd IV and V with eight and three tubercles respectively. Claw without inner tooth. Tibiotarsi with chaetae B4 and B5medium size.
Antennae. Typical of the genus. Dorsal chaetotaxy of Ant III-IV as in Fig. 20 and Table 3b. S-chaetae of Ant IV of medium length and thickened, S5 and S6 slightly longer and thicker than others. Apical vesicle distinct, multilobate (Figs 21, 22). Ventral chaetotaxy of Ant III-IV as in Fig. 23 and Table 3b.
Legs. Chaetotaxy of legs as in Table 1C. Claw without internal tooth. On tibiotarsi, chaeta M present and chaetae B4 and B5 relatively long and pointed (Fig. 33).
Remarks. Endonura turkmenica sp. n. seems to be the closest E. ceratolabralis Smolis et al., 2016 recently described from western part of Iran (Smolis et al. 2016a). They differ in a number of characters: maximum length of body without antennae (in turkmenica 1,45 mm, in ceratolabralis 2,55), location of chaeta E on head (in turkmenica free, in ceratolabralis connected with tubercle Af ), labral formula of chatotaxy (in turkmenica: 0/2,4; in ceratolabralis: 0/2, 2), number of chaetae (L+So) on head (in turkmenica eight, in ceratolabralis nine) and presence/absence of tubercle Di on Th I (in turkmenica absent, in ceratolabralis present). Additionally, chaetae De3 on Th III and Abd I-III are very minute and can be easily overlooked in turkmenica (in ceratolabralis well visible and slightly shorter than De2).

Discussion
Unlike most springtails, members of the family Neanuridae completely lack a molar plate on the mandibles and have suctorial mouthparts. Therefore, they are sometimes called sucking forms in contrast to chewing taxa, where mandibles comprise an outlined structure. The highest degree of simplicity of this part of body can be observed within the subfamily Neanurinae, where the majority of genera and species are characterized by a styliform maxilla consisting of no more than one dentate lamella and a thin mandible, usually tridentate with an apical tooth seldom subdivided. For this reason, authors of taxonomic descriptions have usually devoted little attention to the construction of such elements as mandibles or maxillae. Additionally, characteristics of other mouth structures, e.g. the labrum, are frequently omitted from most papers. Interestingly, observations on the genus Endonura and other Neanurinae show that the apical part of the labrum can be modified, and its shape is constant and characteristic of the species. In the light of these facts, this mouthpart element is very useful and should be added to the list of diagnostic features in the Neanurinae taxonomy.
Up to date, two main types of shapes of the apical part of the labrum have been observed within Endonura and other Neanurinae: nonogival and ogival (Deharveng and Weiner 1984). The latter type, present in two species described herein: E. longirostris sp. n. and E. turkmenica sp. n., is characterized by a strongly tapered and sharp end. What is interesting and noteworthy for this type seems to be generally less widespread but appears to be more common in representatives of the genus living at lower geographic latitudes. It is important to question the reasons for such modifications of the labrum and the causes of such a strong elongation of this structure in some species. It is worth noting that such elongation of the labrum is rather not observed in taxa with the first nonogival type.
Recent observations and studies on the diet of some Neanurinae species probably provide an answer to the above question (Smolis 2009, Hoskins et al. 2015. Apparently, an important, and perhaps primary, food resource for this subfamily are slime molds. Like most Neanurinae, this group of organisms can be found mainly in forest habitats, moist and rich in organic matter, in particular in different kinds of decaying wood. It is highly probable that the observed differences in the shape of the labrum allow some Neanurinae species to feed on certain species of slime molds and, in consequence, to reduce interspecies competition. Undoubtedly, to clarify this intricate aspect of the morphology and ecology of Neanurinae, further studies on the Endonura species with different modifications of the labrum, are needed.